Ann Thorac Surg 2000;70:527-532
© 2000 The Society of Thoracic Surgeons
Original articles: cardiovascular
Intramyocardial impedance measurements for diagnosis of acute cardiac allograft rejection
Robert Pfitzmann, MDa,
Johannes Müller, MDa,
Onnen Grauhan, MDa,
Roland Hetzer, MD, PhDa
a Department of Cardiothoracic and Vascular Surgery, Deutsches Herzzentrum Berlin, Berlin, Germany
Address reprint requests to Dr Pfitzmann, Department of Cardiothoracic and Vascular Surgery, Deutsches Herzzentrum Berlin, Augustenburger Platz 1, 13353 Berlin, Germany
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Abstract
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Background. Measurements of intramyocardial impedance at high frequencies can indicate alterations in cell membranes and intracellular spaces during acute cardiac allograft rejection.
Methods. Fifteen beagle dogs underwent heterotopic heart transplantation and were immunosuppressed with cyclosporine and methyl prednisolone (MP). Impedance was determined twice daily by means of four screw-in electrodes in the right and left ventricle. Transmyocardial biopsies and the intramyocardial electrogram (IMEG) were performed as reference methods. A total of 23 rejection episodes were induced. When acute rejection was recognized histologically and through IMEG readings, the animals were treated with a bolus of 125 mg of methyl prednisolone over 5 consecutive days. Treatment of rejection was controlled by biopsy and IMEG.
Results. All hearts showed a uniform decrease in impedance of about 28.3% ± 5.5% immediately after transplantation, which subsequently reached a stable plateau after 7 to 8 days. Impedance values then remained unchanged as long as rejection was absent. Biopsy findings of grades 1A to 1B (ISHLT) were accompanied by a statistically significant increase in impedance of 12.2% ± 2.5%; of grades 2 to 3A of 19.2% ± 3.2% and of grades 3B to 4 of 27.0% ± 2.9%. Sensitivity was 96%, specificity 91%. Successful treatment of rejection led to a decrease of impedance to the initial levels.
Conclusions. The amount of increase in impedance of high frequencies is a method to stratify acute cardiac allograft rejection into grades like histologically grading. The effectiveness of rejection treatment can also be monitored through impedance measurement. The method is also applicable for telemetric rejection monitoring by means of an implantable device.
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Introduction
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Since the advent of heart transplantation as a routine surgical treatment for heart insufficiency NYHA class IV, the main concern of physicians after surgery has been the early detection of cardiac allograft rejection. There are a number of methods available to detect acute cardiac allograft rejection, such as echocardiography, cytoimmunological monitoring (CIM), surface- and intramyocardial electrogram (IMEG), and the "gold-standard" of transvenous endomyocardial biopsy, but as yet there is no generally accepted noninvasive method for diagnosing acute rejection after heart transplantation. The above-mentioned methods are only reliable for the diagnosis of acute rejection for daily application. The IMEG offers the possibility of daily and continuous rejection monitoring of a patient at home by means of an implantable device without necessitating hospital admission. However, in a few cases, IMEG tracings exhibit certain alterations in amplitude that can be precipitated by many other factors (common colds, influenza, or viral infections) other than rejection. The aim of this study was to develop additional noninvasive monitoring for the diagnosis of rejection after heart transplantation to the IMEG.
The feasibility of impedance measurements in biological tissue has been recognized since the 1800s, mainly for the diagnosis of cell death, and they have been used since the 1900s primarily for the determination of ischemic tissue tolerance [1, 2, 4, 5, 9–22]. Intramyocardial impedance describes the capacitive conductivity and, in turn, the behavior of fluctuations in the resistance of alternating currents in biologically active tissue [8, 15]. According to the Maxwellian potential theory, the impedance of biologically active tissue is dependent upon frequency [8, 15] (Fig 1). Therefore, it is possible to examine various tissue structures of different frequencies [1, 8, 15]. For low frequencies of an alternating current, the cell membrane and the intracellular space (ICS) combine to produce the effect of an insulator. Alternating currents for high frequencies pass through the cell membrane and the intracellular structures, and therefore, demonstrate alterations of the cell membrane and the ICS [1, 3] (Fig 1). In addition to frequency, impedance is dependent upon the material and form of the electrodes, as well as the mode of measurement with either a two- or four-pole configuration [3, 8, 23, 24]. Using the two-pole method, voltage is recorded at the same electrodes to which the current is applied [23]. In contrast, the four-pole configuration allows current application on one electrode pair and impedance measurements on the other, with less of a polarization phenomenon [23, 24]. The effects of polarization must be taken into account at high current densities and for the two-pole configuration, where absolute values of impedance are recorded. These effects are less crucial for day-to-day measurements of impedance, as relative rather than absolute values are of importance. In this study, rectangular impulses were applied to the myocardium and changes in the impulse response curve were measured to determine the level of tissue impedance [2, 4, 6, 8, 9, 22–24].
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Fig 1. The behavior of a current step in biologically active tissue. High frequencies (transient phase) passes the cell membrane and the intracellular space: low frequencies (constant phase) passes only the extracellular space (ECS).
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Material and methods
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Fifteen adult beagle dogs underwent heterotopic neck-heart transplantation. The hearts of immunologically unmatched donor dogs of half the recipient’s body weight were arrested using Bretschneider’s cardioplegic solution and surface cooling. An atrial septal defect and mitral insufficiency were artificially created to drain the blood reaching the left heart by small (Thebesian) veins. The atria were closed by suture, the pulmonary artery was anastomosed to the external jugular vein, and the aorta to the common carotid artery of the recipient dog. The donor heart was planted subcutaneously. Two epimyocardial screw-in electrodes (model 6917 A-T, Medtronic Corporation, Minneapolis, MN) were attached to the myocardium of the right and left ventricle. All electrodes were exited outside percutaneously at the dorsal neck of the recipient dog. Four donor organs were fitted with electrodes 4 weeks before transplantation so as to judge the influence on impedance measurements of the healing of the myocardium after electrode placement and the influence of methyl prednisolone in the absence of acute allograft rejection. All animals were handled according to the German laws of animal care.
Four two-pole and one four-pole configuration for high and low frequency measurements were performed for each dog twice daily. The day-to-day impedance values for high and low frequencies were calculated and presented in a graphic as percentile values (Fig 2–5). Twice daily taken IMEG readings and biopsy served as reference methods. Based upon previous clinical experience, a voltage amplitude reduction of 10% or more in the IMEG was used as an indicator of rejection and a biopsy was then performed. All biopsies were histologically graded according to the International Society for Heart and Lung Transplantation (ISHLT) classification by a pathologist who was blinded to the study protocol. The myocardial biopsies were performed under anesthesia with thiopental (20–40 mg/kg body weight) by reopening the skin incision over the subcutaneous neck-heart. Transmural punch-needle biopsies were taken and the site was oversewn. During autopsy, biopsy samples were taken directly from the circumferences of each electrode to examine the presence of fibrotic tissue around the electrodes. A fibrotic layer with a diameter of more than 1 to 2 mm was designated as fibrosis.
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Fig 2. The spontaneous course of the impedance of high and low frequencies and after treatment with corticosteroids in nontransplanted hearts.
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Fig 3. The impedance course for high and low frequencies of acute rejection ISHLT grades 1A and 3A and their successful treatment.
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Fig 4. The impedance course for high and low frequencies of acute rejection International Society for Heart and Lung Transplantation (ISHLT) grades 2 and 3B and their treatment.
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Fig 5. The impedance course for high and low frequencies of acute rejection International Society for Heart and Lung Transplantation (ISHLT) grades 1B and 4 and their treatment.
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For purposes of immunosuppression, cyclosporine A was begun on the day of operation at an initial dosage of 10 mg/kg body weight twice daily. The dosage was then adjusted to therapeutic whole-blood levels between 400 and 600 ng/mL. Intraoperatively, methyl prednisolone 250 mg was given, with a repeat dose of 125 mg on postoperative day 1. From postoperative day 2 on, cyclosporine A was the only immunosuppressant drug used. Cyclosporine A whole-blood levels were monitored with a whole-blood radioimmunoassay daily. The cyclosporine A application and the drawing of blood samples for whole-blood level monitoring were performed by means of two seperate venous port systems implanted on the right side of the animals’ necks. Rejection therapy was performed after biopsy diagnosis with methyl prednisolone 125 mg over 5 consecutive days.
The first postoperative myocardial biopsy was performed after a therapeutic whole-blood level of cyclosporine A of 400 to 600 ng/mL had been attained, and a stable plateau in the intramyocardial ECG voltage registration had been observed for at least 3 days. When acute rejection was excluded histologically, cyclosporine A whole-blood levels were lowered to about 200 ng/mL in eight cases, to about 120 to 100 ng/ml in eight further cases, and to about 80 to 50 ng/mL in seven others by randomization of the animals to induce acute cardiac allograft rejection episodes. As soon as a 10% intramyocardial ECG voltage drop beneath the baseline was noted, a second biopsy was performed. After histological diagnosis of acute rejection, treatment with methyl prednisolone over 5 consecutive days was begun and cyclosporine A whole-blood levels were again elevated to 400 to 600 ng/mL. A second biopsy was performed to assess the success of the rejection therapy at the end of treatment. Seven dogs had one rejection episode, eight dogs experienced a second rejection episode and subsequent treatment (Tables 1 and 2). Altogether, we induced 23 rejection episodes by alteration of the immunosuppression (Table 1). The 
2 and Kruskal-Wallis tests were used for statistical analysis (Table 3). The results were expressed as means plus or minus standard errors of the mean (Table 2).
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Table 2. Results of Impedance Measurements, Including Means, Single Standard Deviation (1 s), and Percentage Ranges
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Table 3. Relationship Between the Results of Intramyocardial Electrogram, Biopsy, and Impedance for Diagnosis of Acute Rejection
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Results
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The impedance measurements of the four native hearts showed for the two- and four-pole configuration an initial increase in the mean of about 20.3% ± 3.7% (1 standard deviation; range 16% to 25%) for the high and 8.0% ± 1.4% (1 standard deviation; range 6% to 9%) for the low frequencies. After a mean of 10 days (range 7 to 13 days), a stable baseline was attained (Fig 2). The administration of methyl prednisolone 125 mg over 5 consecutive days produced no significant alterations for high and low frequencies of impedance (Fig 2). The mean examination time for the transplanted hearts was 33 days (range 14 to 47 days). The mean total ischemic time was 128 minutes (range 88 to 176 minutes). All hearts manifested a regular sinus rhythm with frequencies between 110 and 150 beats/min after transplantation and showed good contractility. All hearts exhibited an initial decrease in impedance values in the two- and four-pole configuration after transplantation. For the high frequencies, we observed a decrease of 28.3% ± 5.5% (range 20% to 38%) and 12.4% ± 2.0% (range 10% to 16%) for the low frequencies, which eventually reached a stable plateau after 10 days (range 8 to 13 days) posttransplantation (Figs 2 through 5). The reduction of the whole-blood level of cyclosporine A to about 200 ng/ml led to an acute cardiac allograft rejection ISHLT grades 1A to 1B in eight cases (Figs 3 and 5, Table 2). Impedance values showed an increase of 12.2% ± 2.5% (range 8% to 15%) for high and 2.0% ± 1.4% (range -2% to 4%) for the low frequencies. After treatment of rejection over 5 consecutive days, all impedance values reassumed their initial values and the subsequent biopsy manifested no more histological signs of acute rejection. A further reduction of cyclosporine A whole-blood levels to about 120 to 100 ng/mL led to moderate rejection episodes ISHLT grades 2 to 3A in eight cases (Figs 3 and 4). The impedance values for high frequencies showed an increase of 19.2% ± 3.2% (range 15% to 25%) and 4.1% ± 2.0% (range 2% to 7%) for the low frequencies. Rejection treatment, controlled by biopsy, was successful in all cases and the impedance measurements again exhibited their initial (baseline) values (Figs 3 and 4). A reduction of whole-blood levels of cyclosporine A to about 80 to 50 ng/mL led to severe rejection episodes ISHLT grades 3B to 4 in seven cases (Figs 4 and 5). The impedance values for high frequencies showed an increase of 27.0% ± 2.9% (range 24% to 31%) and for the low frequencies of about 6.0% ± 1.6% (range 4% to 8%). Five hearts experienced total recovery after treatment with methyl prednisolon over 5 consecutive days. The impedance values assumed their initial values. After treatment of rejection over 5 consecutive days, two hearts showed impedance values of about 15% over their initial plateau with an involution of rejection in the biopsy. After a second treatment for rejection over 5 consecutive days, biopsy revealed no more signs of rejection, but the impedance values for the high and low frequencies did not reach their initial values and were found to be about 4% above their initial baseline (p = ns). The histological examination of the electrode circumferences (n = 60) revealed fibrotic tissue of 32% (n = 19). The electrodes of the native hearts with fibrotic tissue surrounding the electrode tip showed an initial higher increase of the impedance values of about 7.0% ± 2.1% (range 4% to 8%) for the high and low frequencies. For the impedance of transplanted hearts, we observed an initial stronger decrease of about 5.0% ± 1.4% (range 3% to 6%).
Altogether, the impedance measurements detected 22 of 23 rejection episodes. One rejection episode, grade 1A, was not accompanied by an impedance increase. However, in three cases, the impedance showed an increase of more than 10% without alteration of the IMEG and no signs of rejection in the biopsy. The calculated sensitivity and specificity for the impedance was 96% and 91%, respectively. Sensitivity and specificity for biopsy and IMEG were 100% (Table 3). The impedance measurements for high frequencies were statistically significant for detecting acute cardiac allograft rejection (p = 0.009) but not significant for the low frequencies (p = 0.8).
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Comment
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The initial increase of the low- and, especially, the high-frequency currents in the native hearts can be explained by the development of a current potential caused by tissue injury during electrode implantation (hemorrhage, cell swelling, hypoxia, and necrosis) [1, 2, 15]. The tissue ischemia leads to an accumulation of acid metabolites, that cause closure of the gap junctions and therefore an increase in impedance of the cell membrane and the ICS. This process explains the larger increase in impedance for the high-frequency currents. The varying degree of injury in the region of myocardium in the electrode surroundings after implantation led to varying increases in impedance and, in turn, to the subsequent impedance reductions after healing of the tissue that surrounds the electrodes.
During myocardial recovery, impedance values show a drop to their initial values in direct relationship to the development of fibrotic tissue around the electrodes. Electrodes with marked fibrotic circumferences led to larger increases in impedance than electrodes without or with less fibrotic tissue. This observation correlates well with the results of other studies [9–11, 15, 17]. The application of high-dose corticosteroids after the "healing-in" of the electrodes in the myocardium showed no effect on impedance measurements. Thus it would appear that corticosteroids had no direct or indirect influence on impedance measurements in nontransplanted hearts, especially with regard to their membrane-stabilizing and antiinflammatory effects.
Some studies show an initial increase in impedance caused by ischemia during cardiac surgery with application of cardioplegic solution and surface cooling, followed by a plateau phase without evident alteration in impedance [9–13, 16, 18, 21]. The ischemic period and the plateau phase led to irreversible damage and eventual loss of organ function [9–14, 16–18]. Cardioplegic cardiac arrest leads to an ischemic and anaerobic metabolism, which causes an increase in myocardial impedance [9–14, 16–18]. After termination of ischemia, the impedance values decrease in direct relationship to the period of ischemic stress of the myocardium [11, 12, 14, 16, 17].
In the moment of first impedance measurement in our experiments, the period of acute ischemia of the heart was terminated and thereupon was followed by the reperfusion phase and subsequent recovery. The initial decrease in impedance of transplanted hearts in contrast to initial increase of the native hearts must be seen as a phenomenon of reperfusion and furthermore as an effect of myocardial recovery. After recovery from ischemia and reperfusion edema and after the "healing-in" of the electrodes, the impedance values maintained a stable baseline.
The impedance measurements in our experiments for high frequencies, represented by alterations of the cell membrane and the ICS [1, 15], exhibited remarkable fluctuation. In contrast, the alterations of the impedance at low frequencies, which represent the extracellular space (ECS), were less remarkable. It seems that the development of acute rejection episodes led to significant alterations of the cell membrane and the ICS, which were detectable by impedance measurements at high frequencies. The histologically imposing extracellular edema and lymphocytic infiltration during acute rejection in the myocardium seem to have less influence on impedance measurements at low frequencies. In conclusion, alterations in impedance are more likely to be influenced by alterations in the cell membrane and the ICS during cardiac allograft rejection.
In direct relationship to the reduction of immunosuppression and the resulting severity of acute rejection, the cell membrane and the ICS incur varying degrees of damage and, consequently, the myocardial impedance increases. The increase in impedance can be explained by damage to the cell membrane through cellularly-induced and humoral rejection. In addition, mediators of inflammation and antibodies may damage the ion channels and lead equally to the development of intracellular edema and cell swelling. Conceivably, such damage to subcellular structures may lead to an additional increase in impedance. In addition, severe rejection episodes that induce focal myocardial necrosis followed by fibrosis cause an increase in impedance. The treatment of rejection with glucocorticosteroids in all cases led, with the exception of two rejection episodes of ISHLT grade 4, to a drop in impedance to their initial values. This indicates irreversible structural and functional damage of the myocardium, which was confirmed by histological findings.
The same course of impedance, as in our experiments, was shown by another study with an initial decrease in impedance of 30% after human heart transplantation [25]. In the same way Fourcades and Descotes [15] described in 1975 intramyocardial impedance with two frequencies in dogs after heart transplantation and the development of acute rejection. They obtained an initial reduction in intramyocardial impedance of about 45%. The results of our examinations of the myocardium have shown that rejection-induced effects on the cell membrane and the ICS lead to distinct alterations in impedance for high-frequency currents. Alterations in the ECS during rejection seem to have less influence on impedance values at low frequencies.
The results of impedance measurement for the course of 23 acute rejection episodes and their treatment assume that intramyocardial impedance at high frequencies can indicate alterations of the cell membrane and the ICS and, therefore, provide evidence of acute allograft rejection. The advantage of this technique in contrast to IMEG is that the amount of increase of impedance is a parameter for grading acute rejection, which is similar to the graduation criteria used in biopsy (Table 2). The success of treatment of rejection can also be monitored by the course of impedance. The impedance measurement is applicable for telemetric monitoring by means of a specially fabricated implantable device (Cardiotechnica Corp, Berlin, Germany). The impedance method, in addition to IMEG, makes the diagnosis of acute cardiac allograft rejection more reliable.[7]
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Accepted for publication February 10, 2000.
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Abstract
Introduction
