endocarditis in patients with bioprostheses: pathology and clinical correlations
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Endocarditis in patients with bioprostheses: pathology and clinical correlations
Zussa c‘. Galloni MR, Zattera GF, Pansini S, Di Summa M. Poletti GA, Ottino G. Morea M. Endocarditis in patients with bioprostheses: pathology and clinical correlations. Int J Cardiol 1984:6:719-732.
We studied 13 porcine bioprostheses removed from patients with endocarditis at
our institute during the last 4.5 years. All bioprostheses had been removed at
reoperation and were analyzed using anatomical and histological techniques. Each
bioprosthesis was found to have developed rather constant lesions which were not
related to the type of bioprosthesis. The stage of infection was not related to the
duration of implantation. The presence of perivalvular abscesses was an ominous
finding, often being the seat of persistent endocarditis. Our good clinical results of
reoperation lead us to suggest that this be performed early once vahular or prosthetic
malfunction is detected. Bioprostheses are, in our experience, the best choice in the
surgical treatement of prosthetic valve endocarditis.
(Key words: valve replacement; histology: electron microscopy)
Introduction
Endocarditis is. in our experience and of others. one of the main causes leading to reoperation during the first 7 years after cardiac valve replacement with bioprosthe-
0167.5272,'X4,~'$03.00 ’ 1984 Hsewer Scwnce Puhlt\hcrs H V
ses [l-10]. At our institute we always considered titc Goprosthesis as the first choice
in valvular surgery, regardless of the causes of the valvulopathy. because of their IOU
incidence of thromboembolic complications and their excellent hemodynamic per-
formance. The purpose of this study was to search for any correlations between the
clinical data and the pathological changes observed in bioprostheses removed from patients affected by endocarditis. In this way we hoped to establish the best
therapeutic approach to this complication.
Materials and Methods
In the period between January 1979 and June 1983 we performed 1107 valvular surgery operations in which 1045 bioprostheses and 201 mechanical valves were
implanted. During the same period we observed 22 patients suffering from endo-
carditis; in this group, among the 17 patients with a porcine bioprosthesis. 13 needed a new bioprosthetic valve replacement, as did 3 of the 5 patients with a mechanical
valve. Occurrence rates of post-operative endocarditis were 0.7% per patient-year
and, respectively, 0.6% per bioprosthesis-implant-year and 1.5% per mechanical valve-implant-year. The diagnoses were based on at least two of the following
criteria: (1) typical clinical signs (fever. embolism, splenomegaly, new cardiac
murmur), (2) at least two positive blood cultures and/or positive cultures from the annular or bioprosthetic tissue obtained at reoperation. and (3) pathological evi- dence of endocarditis. This study deals with the 13 above-mentioned patients who.
from an etiological point of view. could be divided as follows: two (cases 3 and 12) had endocarditis on a previous mechanical valve implanted in other surgical centers,
Fever. splrnomegaly. new cardiac murmur. M = mitral: Ao = wrtic: T = tncuapld: AF = atriat flhritlatlon;
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one (case 8) had native valve endocarditis while the remainder were affected b> non-infective cardiac disease. Ten were male and three were female. Ages ranged from 25 to 5X years (42 & 12.3). The affected porcine bioprostheses were in aortic.
mitral and tricuspid position in seven cases, five cases and one case, respectively.
The relevant clinical findings are listed in Table 1. Two patients (cases 7 and 13)
were reoperated upon because of suspected primary tissue failure, one having had a
previous mild bout of fever and a new cardiac murmur, the other having had only a new cardiac murmur. The bioprosthescs of these two patients showed bacterial
colonies: in addition in case 7 streptococci were cultured from samples taken from
the valve during operation. Seven patients were operated upon as emergencies or with urgency (within 72 hr of presentation at our surgical center). The remaining
patients underwent elective valve replacement. Two patients died within 30 days after surgery because of respiratory insufficiency and multiple preoperative mycotic emboli. Three had persistence of endocarditis while all others promptly recovered
from the infective process. Long-term follow-up (6 to 55 months. 22.9 & 17.7) shows no late deaths.
The removed bioprostheses were fixed in 3’0 glutaraldehyde in phosphate buffer
(0.1 M; pH 7.3) and were X-rayed with mammographic films (25 mA. 37 kV, 0.3 .sec). Gross and low power examination was carried out using a stereomicroscope in
transmitted polarizing light. Specimens from each bioprosthetic leaflet were pre-
parec for optical microscopy by post-fixation with 109’ neutral buffered formalin. They were then embedded in paraffin and sectioned at 5 pm thickness. The sections
were stained with hematoxylin-eosin. Weigert-Van G&on. Gram, Grocott and Von
Kossa techniques. Further specimens were taken for scanning electron microscopy and were dehydrated in a graded alcohol series. critical point dried in liquid CO,
and sputter coated with gold. They were examined with a Cambridge Stereoscan 100 scanning electron microscope.
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Results
Operative Findings
l‘hrombotic Vegetations
Thrombntic vegetation\ \vere variable in distribution and size in the three Itsatlas
of valves inserted in either atriowntricular or aortic position (Table 2). there king
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no significant difference between inflow and outflow surfaces in either position. Massive thrombosis (covering all the area of at least one leaflet) was found in three
of the five cases of streptococcal etiology. This finding was not related to either the
position of the valves or the duration of implantation or the duration of endocardi-
tis. From the morphological viewpoint (excluding the fibrous layer which is the
normal product of the biological interaction between prosthetic valve and host) we observed two main patterns of thrombus considered likely to be of inflammatory
origin. One had a friable, cauliflower-like form (Fig. 1). and the other a Iaminar. smooth and compact one. The Iaminar thrombus in two cases showed finger-like
appearance due to various fibrinous layers lying over each other.
Lacerations
Tears were present in six of seven bioprostheses inserted in aortic and in three of six in atrioventricular position. Table 2 shows the distribution of the various types of
tears in each bioprosthesis according to the classification suggested by Ishihara et al. [l I]. Typically. type I lesions (tears involving the free edges) were close to the nodules of the leaflets. In three of these, the confluence of two such tears caused the loss of the nodule (Fig. 2). Radiographs show calcifications in 80’3 of lacerated
leaflets (12/l 5).
Calcification
Calcification was found in 3X.5? of left cnfonary leaflets (S/13) and in 53.8% 01
the other two leaflets (14/26); 6?.lF of calcified leaflets were also torn. Calcium was found both in leaflets and thrombi. vq ing from small granules to rnah.si\,e deposit>
which immobilized the affected leallt’t~ ( Fig. 3).
Inflammatop Cell Infiltration
This was present in 76.90; of leaflets. being present on both the surfaces and Lvithin the inner connective tissue layers (Table 3). In one case. when the valve had
been removed early (case 10). abundant deposits of inflammatory cells were found onlv on the surface. The inflammatory infiltrate wx made up of macrophuges.
Fig. 3. Case 8. Radiography of massive calcific deposits
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neutrophils, plasma-cells. giant polynuclear ce1l.s and. in a Gngle case. eaainophils
(Fig. 4). These cells uere always present in the thrombotic \‘tb loetationa superimposed
on both surfaces of the bioprosthesis.
Etiological Agents
They were identified in nine valves. being located deep in the leaflets in se\vn: this location corresponds to the third stage of bioprothetic infection evolution
described by Ferrans and colleagues [12]. Histology showed bacterial colonies within the biological parts (leaflets and aortic wail) of the bioprostheses and in the thrombi (Fig. 5). Often these colonies lay close to areas of altered connective tissue huch a:, homogenization. altered staining and cavities. These features were also demonstrated in the two cases reoperated because of presumed primary tissue failure. Scanning
Fig. 5. Case 7. Bacterial colonies near the outflow surface of the non coronary leaflet (Gram stal
magnification 117 X ).
Fig. 6. Case 12. Bacteria observed in the right coronary leaflet, Inflow surface (SEM. magnification
4511X).
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clrctron microscopy revealed the bacteria on the surfaces of these specimens (Fig. 6). Case 1 (with mycotic etiology) was characterized by an onion-like layered thrombus (Fig. 7). Scanning electron microscopy showed this to consist mainly of fungal hyphae, with a shape characteristic of their phasic growth. Rough and brush-like
areas were found with exposed hyphae (Fig. 8) and other areas with smooth fibrin.
Connective Tissue Alterations
Loosening and disruption of the fibrous tissue layers were found in all valves which had been implanted for at least 2 months. The only case without these changes had been implanted for 1 month only.
F’lg. 7. Car 1. Mymtu mien-lihe layered thrombus infiltrating the leaflet (arrows) (Grocott stain. m.ignlfiution 29 x ).
Discussion
We noted that infection of bioprosthetic valves is characterized by rather constant and comparable morphologic lesions no matter which type of valve (Hancock,
CarpentierEdwards, Liotta) had been used. Nevertheless. some etiological agents
produced more specific lesions such as thrombosis, which is always present as vegetations in the mycotic infection whilst perivalvular abscesses are more frequently associated with Srqlz~~lococ~cus infections [13,14]. The stage reached by the infection was not related to the duration of implantation, to the duration of endocarditis or to any particular etiological agent. The pathological findings and the clinical evolution
are similar in bioprosthetic and native valve endocarditis [2,3,5-7,12.13.15--IS]. This persuaded us. therefore, to adopt the same therapeutic approach for bioprosthetic and native valve endocarditis. Thus, in the presence of either valvular or prosthetic malfunction, we usually suggest early operation because we agree that. in the presence of a significant hemodynamic dysfunction, be the patient symptomatic or not. any surgical delay could prove to be useless or even dangerous [1.14,19---221. The less dramatic evolution of the endocarditis on a bioprosthetic valve compared with that when there is involvement of a mechanical valve. is rather typical; from our viewpoint. such behavior could depend on the presence. in the bioprosthesis. of three
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moving components all of which are very unlikely to malfunction at the same time. Bioprosthetic endocarditis. in our and others’ experience, is rarely complicated by
perivalvular abscesses and so by perivalvular leaks; on the contrary they are frequent in mechanical valve endocarditis and cause the rapidly progressive hemodynamic deterioration of the patients [335,8,13,19]. Moreover abscesses are the most frequent
cause of persistence of the infection; in fact, among our four cases of annular abscesses in bioprosthetic valve endocarditis, two had developed during a previous
mechanical valve endocarditis. Furthermore, they produce annular alterations that,
after valve replacement, may result in later paraprosthetic leaks even if the infection is eliminated. Finally the validity and effectiveness of our therapeutic approach is
confirmed by the good results we achieved in the surgery of the native valve
endocarditis. In fact, at our institute, 21 patients affected by active native valve
endocarditis received 17 bioprostheses and 4 mechanical valves (one double valve
replacement) and one patient underwent a conservative procedure: among the 19
patients discharged from hospital, we observed progressive hemodynamic deteriora-
tion, that necessitated valve replacement in only the patient previously treated with the conservative procedure. In the other patients the endocarditis resolved. Late
follow-up showed reinfection after 2 years of well-being in one, a drug addict. Thus far we are satisfied with our results (2 deaths in 13 cases of bioprosthetic infection).
We suggest that the present results support our choice of bioprostheses as the optimal valve for the surgical treatment of both native and prosthetic valve endo- carditis.
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