Interact CardioVasc Thorac Surg 2007;6:772-777. doi:10.1510/icvts.2007.159426
© 2007 European Association of Cardio-Thoracic Surgery
ESCVS article - Cardiac general |
Causes of repeated remodeling of left ventricle after Dor procedure
Vladimir M. Shipulin*,
Vitaly A. Kazakov,
Irina V. Suhodolo,
Evgeny V. Krivoshekov,
Alexander A. Lezhnev,
Boris N. Kozlov,
Valery Ch. Vaizov and
Andrey A. Miller
Cardio-vascular Department, Tomsk Institute of Cardiology, Kievskaya street 111a, Tomsk, Russia, 634012
Received 20 May 2007;
received in revised form 28 August 2007;
accepted 29 August 2007
 Presented at the 56th International Congress of the European Society for Cardiovascular Surgery, Venice, Italy, May 17–20, 2007.
*Corresponding author. Tel./fax: +7 3822 555483.
E-mail address: shipulin{at}cardio.tsu.ru (V.M. Shipulin).
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Abstract
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Objective: To reveal morphological factors causing unfavorable follow-up outcome of surgical treatment of patients with ischemic cardiomyopathy (ICMP) and with left ventricle (LV) aneurysm according to the data of intraoperative biopsies of LV myocardium and right atrium (RA) auricle. Methods: The object of the study was to examine biopsy material of LV myocardium and RA auricle from 36 patients with ICMP. Clinical criteria of patients' inclusion into the study were: ESI LV >80 ml/m2, EDP LV >30 mmHg, LV EF <40%, presence of akinetic and dyskinetic areas in LV, angina of II–IV class CCS, heart failure of II–IV class NYHA. The following morphometrical parameters were estimated for revelation of postoperative remodeling risk factors: parenchymal–stromal ratio (PSR), trophic index (TI), pericapillar diffusion zone (PDZ), Kernogan index (KI) and specific volume of granules of natriuretic factor (NUF) in atrial cardiomyocytes. Results: In all the patients LV EF increased significantly (from 36.4±4.1% to 46.3±4.2%) (P<0.05) in the early postoperative period; LV EDI decreased (from 139.3±11.2 ml/m2 to 108.4±8.9 ml/m2) (P<0.05). In the follow-up period (one year) all the patients were divided into two groups: in 28 patients (the 1st group) volume of the cavity, contractile function of LV remained satisfactory. In the other eight patients (the 2nd group) there was significant decrease of LV EF (up to 33.9±10.2%) due to increase of LV EDI [up to 129.2±10.1 ml/m2 (P<0.05)]. Grade of MR preoperatively was 1.21±0.5 and 1.47±0.9, correspondingly, for the patients with positive and negative changes in the follow-up postoperative period. Drawing morphological parallels of postoperative heart remodeling in patients with ICMP showed that diffusive, lymphocytic-macrophage inflammatory infiltration of myocardial stroma in combination with severe fibrosis (PSR<1.5), low TI (<0.015) and greater value of PDZ (>1000 µm) and KI (>1.6) of LV myocardium are the factors connected with unfavorable follow-up results of surgical treatment. Moreover, we showed an inverse correlative relationship between content of NUF granules in the cardiomyocytes of RA auricle and the outcomes of the Dor procedure. Conclusions: Thus, a combination of the foregoing features is a morphological predictor of postoperative heart remodeling in patients with ICMP.
Key Words: Ischemic cardiomyopathy; Left ventricular reconstruction; Pathomorphological predictors
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1. Introduction
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Ischemic heart disease (IHD) still remains one of the most widely spread, progressive and prognostically unfavorable diseases of the cardiovascular system. Ischemic cardiomyopathy (ICMP) preconditioned by diffuse atherosclerosis of coronary arteries and manifested in cardiomegaly and symptoms of congestive heart failure develops in patients with IHD in 10–35% of the cases. The remodeling process is a combination of changes in shape, cavity volumes and postinfarctive heart myocardium mass in response to pronounced inadequet hemodynamic conditions of its functioning not connected with elongation of sacromeres, which is a pathomorphological substrate of chronic heart insufficiency [1, 2]. Coronary artery bypass grafting (CABG), repair of LV shape and volume and mitral valve annuloplasty became widespread as methods of complex surgical treatment of patients with postinfarction heart remodeling [3–11]. Nevertheless, according to the literature, repeated LV remodeling occurs in 12–25% of the literature in the follow-up period. In these cases heart chambers' sizes and hemodynamic values return to preoperative level and sometimes exceed it [12–14]. Patients with potentially unfavorable outcome of surgical LV remodeling should be candidates for initial heart transplantation instead.
The question about preoperative prognosis of surgical treatment outcome in the follow-up period remains unanswered. LV wall kinesis [9], high pressure in parts of the right heart [6], quantity of viable myocardium [4] and presence of mitral regurgitation [9, 15–17] were considered as possible preoperative parameters connected with the risk of progressing LV remodeling. Thorough selection of the patients before surgical treatment outcome will allow increasing efficacy of the given tactics of operative intervention.
Myocardium is a unique tissue which consists of highly differentiated cells – cardiomyocytes having a number of morphological peculiarities when normal and responsible for a set of non-specific structural changes in the pathomorphosis of cardiovascular diseases. The first search for morphological predictors of postoperative heart remodeling in cardiomyopathies began approximately 7–10 years ago when scientists started to analyze the course of the postoperative period and assess the morphofunctional condition of LV myocardium using intraoperative biopsy data. Unfortunately, results of these few studies are absolutely controversial. Moreira et al. [18] relate an average value of LV myocardium cardiomyocytes diameter exceeding 22 µm to the factors connected with unfavorable results of surgical treatment of the patients with dilated cardiomyopathy in the follow-up studies. On the contrary, Popovic et al. [19] have not found correlation between preoperative myocardial morphology and its postoperative function, which the authors explain by too narrow coverage of morphometrical methods of study.
The objective of the given study is to draw clinical-morphological parallels of postoperative LV remodeling in patients with ICMP who underwent surgical treatment.
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2. Patients and methods
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This study was approved by the Local Human Research Ethics Committee, Tomsk Institute of Cardiology, Russia. Informed consent was obtained from all patients.
2.1. Study population
In our clinic, 220 operations for reconstruction of shape, volume of cavities and coronary blood flow were carried out in patients with ICMP during the period from 1991 to 2007. In 135 of them the Dor procedure was performed and in 85 – linear plasty described by D. Cooley. All the procedures were accompanied with CABG. Hospital mortality was 7.7%.
Thirty-six patients with previous large-focal myocardial infarction and with LV systolic and diastolic dysfunction were enrolled in the study. From 2003 to 2006, all the patients with previous large-focal infarctions and with LV systolic and diastolic dysfunction were subjected to surgical treatment for IHD and heart insufficiency. Surgical LV geometry repair by Dor procedure in combination with CABG was performed in 36 patients. Their survival after operations was not <1 year. The key clinical characteristics of the patients enrolled in the given study (shown in Table 1) were the following: end-systolic index (ESI) LV >80 ml/m2, ejection fraction (EF) LV <40%, end-diastolic pressure (EDP) LV 30 mmHg, presence of dys- or akinetic LV anterior wall and/or ventricle septum, angina II–IV CCS, heart failure II–IV NYHA, duration of IHD from 1 to 10 years. The average number of affected coronary arteries was 3.6±1.2 and mitral regurgitation (MR) grade – 1.51±0.92. A peculiar characteristic of each operated patient was myocardial infarction in the region of anterior descending artery previously (Table 1).
2.2. Surgical technique
The operations were carried out with cardiopulmonary bypass at normothermia and cold antegrade cardioplegia with Custodiol®. Standard heart anesthesia was used. LVR was performed in accordance with V. Dor's recommendations [20]. The LV incision was made in parallel with ventricular septum at a distance from the left anterior descending artery which was always shunted with LITA, even in the cases of lack of peripheral bed for septal artery revascularization. Thrombus was extracted; scar tissue of LV in aneurysm was resected. Radiofrequency ablation was used in patients with a history of ventricular tachycardia. A cardiovascular patch (GORETEX, GORE INC., USA) was used for endoventricularplasty, which was sewed to purse-string sutures put on the edge of infarction scar. To avoid creating too small a cavity of LV we used a homemade oliva sizer 60 or 80 cm3.
Concomitant CABG was performed where targeted arteries had been demonstrated. The heart was de-aired in the usual manner. A mean 2.3±1.0 grafts were anastamosed and the left internal mammary artery was utilized in 36 (100%) patients. Mean cross-clamp time was 72±23 min and mean of cardiopulmonary bypass time was 115±36 min.
2.3. Morphological examination
Biopsies of myocardium of RA auricle and of the LV myocardium (n=36) were taken from all the patients intraoperatively. Biopsy of LV was taken after plasty and resection of scar tissue from the rest of the viable myocardium. At preparation of histological samples a standard method was followed. It included biopsy material fixing in 10% solution of neutral formalin, dehydration in ethanol of graded concentration and pouring the material into paraffin. Histological biopsy specimens were colored with hematoxylin-eosin by Malory method and were studied with the help of general and polar microscopy. Myocardium of similar heart parts of 15 patients was subjected to electronic-microscopic study. For transmission electron microscopy LV and RA auricle myocardium samples were fixed in 2.5% glutaraldehyde buffered in 0.1 M Na cacodilate (pH 7.4) for 2.5 h at 4 °C, washed twice in 0.1 M Na cacodylate buffer (pH 7.4) for 15 min at room temperature, postfixed in 1% OsO4 in 0.1 M Na cacodylate (pH 7.4) for 2 h at room temperature, washed twice in distilled water for 15 min at room temperature, and dehydrated through a graded ethanol series into acetone and embedded in Epon-Araldite. Thin sections (60–100 nm) were stained with 2% (w/v) uranylacetate in 50% (v/v) ethanol followed by Reynold's lead citrate and examined in a JEM-100 CX II electron microscope operating at 80 kV.
For quantitative characteristic of correlations of myocardium parenchyma, stroma and microcellular capillary bed, with the purpose to reveal risk factors for postoperative heart remodeling, the following morphometrical parameters were evaluated: parenchymo–stromal ratio (PSR), trophic index (TI) and pericapillar diffusion zone (PDZ). For quantitative characteristics of microcellular vessels' bed condition and their volume capacity Kernogan index (KI) was calculated. Mitochondrial–myofibrillar ratio (MMR) and specific volume (Vv) of atrial natriuretic peptide granules were calculated. MMR is a ratio of mitochondria Vv to myofibrils Vv. Diameter of cardiomyocytes was measured.
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To compare morphometrical parameters, myocardium of similar heart parts were taken from 20 people (17 men, 3 women) of comparable age who died of acute injury without signs of cardiovascular pathology. The study was approved by the Ethics Committee at Tomsk Institute of Cardiology.
2.4. Imaging data
Detailed preoperative and postoperative echocardiographic data were available for 36 (100%) patients. Examinations with a ‘PHILIPS EnVisor C HD’ machine were done repeatedly before the operation and during one year after the operation.
2.5. Statistical analysis
Calculation of tissue and cell stereological parameters was based on data of general light and electronic microscopy. Results are shown as a mean value (M) and error of mean (m). Reliability of the obtained values was checked with non-parametric criterion by Van-de-Varden. Difference of the values in the compared groups was considered reliable at P<0.05. There was assessed reliability of differences of relative frequency of myocarditis signs in groups of patients with positive and negative changes of follow-up results of ICMP surgical treatment.
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3. Results
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Analysis of follow-up results of surgical treatment allowed division of the patients into two groups. The first group included 28 patients with LV EDI at postoperative level within one year after the surgery. The remaining eight patients were included into the 2nd group with repeated LV remodeling whose LV EDI was not changed or exceeded preoperative values within one year after the operation (Table 2). One year after operative treatment LV EF was significantly higher and values of EDI and LV ESI significantly lower than initial values in the 1st group of patients. On the contrary, in the 2nd group of patients, statistically significant decrease of LV EF due to increase of LV EDI and LV ESI in comparison with preoperative values was noticed (Table 2). In the 1st group, values of heart insufficiency NYHA were significantly lower in one year and in the 2nd group – significantly higher than initial preoperative values (Table 2).
Retrospective analysis of the initial clinical characteristic of the patients involved in the study showed that the groups of patients did not differ significantly in basic parameters defining progression of post-infarction LV remodeling (such as EDI, ESI, degree of heart insufficiency and EF). It is necessary to note that among the patients from the 1st group, there was a higher percentage of patients having a single myocardium infarction in the case history, whereas in the 2nd group, patients with multiple myocardium infarctions prevailed. Class III NYHA prevailed in both groups; diabetes mellitus occurred in the 1st group of patients more often – in six patients (21.4%), while in the 2nd group – in two patients (25.0%). Thirteen patients (46.4%) with favorable postoperative period did not have mitral regurgitation, eight (28.5%) and seven (25.0%) of the patients had I and II grades, correspondingly. Grade I of mitral regurgitation in the 2nd group was seen in one patient (12.5%), II – in four patients (50%), III – in one patient (12.5%) and only two patients (25%) had no mitral regurgitation.
We found that density of vessels distribution in LV and RA myocardium in patients with ICMP was significantly reduced in comparison with control cadaver material of patients who died of acute injury with no signs of cardiovascular pathology. Irrespective of blood vessels' diameter disturbances of hemodynamics were noticed everywhere: perivascular edema, venous plethora (Fig. 1), desolation and spasm of arterioles and small arteries.
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Fig. 1. LV myocardium of the patients with ICMP. Perivascular edema (a), venous plethora (b). Dyed with hematoxylin and eosin. x200 (a) and 500 (b).
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The microcircular vessel bed was plethoric, there was often occurrence of stasis of erythrocyte in capillaries, pericapillaries and arterioles. In other capillaries noticed to have endothelial cells, nuclei bulging into the lumen of capillaries resulted in their diminished volume capacity and level of myocardium metabolism (Fig. 1).
Mixed lymphocytic-macrophage infiltrate (>14 per 1 mm2 of tissue by Marburg classification–World Heart Federation Classification and Consensus Conference on the Histo- and Immunohistopathology of Myocarditis, Marburg, April 28–29, 1997 and on Viral Cardiomyopathy, Marburg, October 3–5, 1997) in LV myocardium stroma was found in all the patients of the 2nd group and in 18 out of 28 patients (64.3%) of the 1st group, and that was considered as myocarditis (Fig. 2).
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Fig. 2. LV myocardium of the patients with ICMP. Mixed (lymphocytic-microphage) stromal infiltrate. Dyed with hematoxylin and eosin. x150 (a) and 700 (b).
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Fibrosis in LV myocardium was moderate as a rule (Marburg classification) or mild in the 1st patient group and predominantly severe and, in rare instances, moderate in the 2nd group. In half of the cases among the patients of the 1st group and in 100% in patients of the 2nd group infiltration had a diffuse picture, less often – focal or confluent. Moreover, in five (62.5%) patients with repeated LV dilatation and in eight (28.5%) patients with favorable follow-up results of surgical treatment, infiltrate with a similar picture was found in the myocardium of RA auricle. At the same time, fibrosis was 1–2 grades lower than in myocardium by the same classification. In polarized light, alongside with unchanged areas of LV and RA auricle myocardium cardiomyocytes cytoplasm, there were observed affected areas with prevalence of subsegmental contractions, contractions of I, II less often of III degree, separate areas of intracellular myocytolysis and primary clump disintegration of myofibril and cardiomyocyte fibrosis. Mentioned changes had a mosaic picture.
At electronic-microscopic study of LV and RA auricle myocardium samples, myocardial cell nuclei had an awkward scalloped shape with multiple invaginations of a nuclear membrane; aggregation of chromatin was noticed.
Electronic-microscopic study revealed alternative insufficiency of cardiomyocytes of both LV myocardium and RA auricle. Most often, there were noticed contractile types of cardiomyocyte myofibril lesions of different grades as well as primary clump disintegration.
Alterative insufficiency of cardiomyocytes in conditions of chronic myocardial ischemia is combined with their plastic insufficiency which manifests as myofibrils ‘melting’ and their inability to restore proper size, dispersion and segregation of fibrillar and granular components of a nucleus, widening of perinuclear space, disturbance of neogenetic myofibril orientation and their excess elongation.
Thus, morphofunctional condition of LV myocardium and RA auricle in patients with ICMP completely reflects clinical severity of the myocardial disease. Intensity and combination of basic forms of cardiomyocyte lesions vary in different patients, which is quite explicable since coronary artery lesions become the reason for myocardium ischemia. Its influence on contractile function of a heart muscle is different in different patients and depends on the kind of coronary artery lesions (severity and longevity of ischemia), reperfusion (time and completeness of blood flow restoration) and reaction of myocardium, which, apparently, has significant flexibility in this response as well as on peculiarities of myocardium of each patient. With this, morphofunctional condition of RA auricle myocardium completely reflects morphofunctional condition of the LV myocardium, i.e. is a kind of a ‘mirror’ of the latter.
It is impossible to reveal morphological predictors of postoperative heart remodeling based only on the data of descriptive morphology. To achieve the stated purpose, it is necessary to take into account quantitative values which allow evaluating conditions of function of a structural heart unit – the entire myocardium.
Statistical analysis of the morphometrical data given in Table 3 showed that parenchymo–stromal ratio and TI of RA auricle and LV myocardium is significantly lower in the patients with postoperative heart remodeling, TI in these patients was 8–12 times lower than in those of the control group. On the contrary, PDZ and KI of RA auricle and LV myocardium were higher in the patients of the 2nd group; the PDZ in them was 14–20 times greater than in the control group. The same values in the patients in the 1st group were much more favorable than those of the 2nd group, but they differed significantly from the data of control studies. Mean values of cardiomyocyte diameter of RA auricle and LV myocardium did not differ significantly in the patients with different results of operative treatment but exceeded the data from the control group (Table 3).
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Table 3 Parenchymo–tromal ratio, trophic index, pericapillar diffuse zone, Kernogan index, and cardiomyocytes diameter of left ventricle and right atrium auricle myocardium in the patients with ischemic cardiomyopathy with different follow-up outcomes of surgical treatment, Van-der-Varden criterion, M±m
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Out of 15 patients whose LV and RA auricle myocardium was subjected to microscopic study, four patients had postoperative heart remodeling while in 11 patients shape and contractile function of the LV remained satisfactory. Statistical analysis of ultrastructure morphometrical data showed that specific volume of cardiomyocytes myofibrils was lower and specific volume of cardiomyocytes mitochondria of both LV and RA auricle myocardium was higher in the patients with unfavorable follow-up results of surgical treatment.
The consequence of these changes is a higher mitochondrial–myofibrillar ratio. Specific volume of granules of atrial natriuretic peptide of RA auricle cardiomyocytes is decreasing significantly as heart insufficiency progress which reflects, supposedly, depression of all synthesizing processes in a cell. Specific volume of cardiomyocyte nuclei does not change significantly (Table 4).
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Table 4 Morphometrical values of cardiomyocytes ultrastructures of LV and RA auricle myocardium in the patients with ICMP with different results of surgical treatment, Van-der-Varden criterion, M±m
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4. Discussion
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In the course of our study, in 22.2% of the cases we obtained unfavorable outcome of complex surgical treatment of LV ischemic remodeling, which corresponds to the data presented by other authors [4, 7, 15]. In a year of postoperative observation in this group, irrespective of surgical treatment, LV cavity size exceeded preoperative values. Having divided the groups based on follow-up results of surgical treatment and comparing their initial parameters, we did not find significant difference in preoperative examination data and the method of operative treatment. In other words, we did not reveal any reliable clinical or echocardiographical predictors of postoperative LV remodeling. In our study, systolic and diastolic LV sizes as predictors of postoperative remodeling described by other authors were not proved [4, 9, 15, 16]. At the same time, comparison of these morphometric values, describing quantitative relations of myocardium parenchyma, stroma and microvascular bed, and follow-up results of surgical treatment allowed us to reveal morphological predictors of postoperative LV remodeling. They were: presence of signs of myocarditis in combination with pronounced fibrosis (parenchymo–stromal ratio <1.6), low trophic index (<0.015) and high values of pericapillary diffuse zone (>1000 µm), Kernogan index (>1.5) and mitochondrial–myofibrillar ratio (>0.050).
Presence of myocarditis in the RA auricle myocardium means presence of inflammatory infiltration in LV myocardium in 100%. This fact may also be referred to as a morphological predictor of secondary heart remodeling and heart failure progress in patients with ICMP in the follow-up period.
Revelation of the mechanisms of heart failure progress after intracardial correction and revascularization would allow narrow indications for complex surgical treatment.
In some of the patients, standard methods of surgical treatment (total myocardial revascularization, LV volume reduction and mitral regurgitation correction) do not result in involution of this pathological process. In the future the determination of prognosis of postoperative heart remodeling based on complex evaluation of functional morphology of myocardium preoperatively will allow avoidance of unfavorable follow-up results of surgical treatment. At the same time it remains unclear how to evaluate the degree of intensity of such morphofunctional changes in every case based on clinical and instrumental data.
There are several limitations to our study, including the size of the patient cohort and the length of follow-up, and the fact that preoperative myocardial viability was not precisely evaluated by MRI and no other hemodynamic studies besides echocardiography were performed postoperatively.
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Abstract
1. Introduction
