Original Article
The Prognostic Value of C-Reactive Protein and Serum Amyloid A Protein in Severe Unstable Angina
N Engl J Med 1994; 331:417-424August 18, 1994
- Abstract
Background
The pathogenesis of unstable angina is poorly understood, and predicting the prognosis is problematic. Evidence suggests that there may be active inflammation, possibly in the coronary arteries, in this syndrome. We therefore studied the prognostic value of measurements of the circulating acute-phase reactants C-reactive protein and serum amyloid A protein, which are sensitive indicators of inflammation.
Methods
We measured C-reactive protein, serum amyloid A protein, creatine kinase, and cardiac troponin T in 32 patients with chronic stable angina, 31 with severe unstable angina, and 29 with acute myocardial infarction.
Results
At the time of hospital admission, creatine kinase and cardiac troponin T levels were normal in all the patients, but the levels of C-reactive protein and serum amyloid A protein were ≥ 0.3 mg per deciliter (exceeding the 90th percentile of the normal distribution) in 4 of the patients with stable angina (13 percent), 20 of the patients with unstable angina (65 percent), and 22 of the patients with acute myocardial infarction (76 percent). The 20 patients with unstable angina who had levels of acute-phase reactants ≥ 0.3 mg per deciliter had more ischemic episodes in the hospital than those with levels <0.3 mg per deciliter (mean [±SD] number of episodes per patient, 4.8 ±2.5 vs. 1.8 ±2.4; P = 0.004); 5 patients subsequently had a myocardial infarction, 2 died, and 12 required immediate coronary revascularization. In contrast, no deaths or myocardial infarction occurred among the 11 patients with levels of acute-phase reactants <0.3 mg per deciliter, and only 2 of them required coronary revascularization. Among the patients admitted with a diagnosis of acute myocardial infarction, unstable angina preceded infarction in 14 of the 22 patients (64 percent) with levels of acute-phase reactants ≥ 0.3 mg per deciliter but in none of the 7 patients with levels <0.3 mg per deciliter.
Conclusions
Elevation of C-reactive protein and serum amyloid A protein at the time of hospital admission predicts a poor outcome in patients with unstable angina and may reflect an important inflammatory component in the pathogenesis of this condition. .
Media in This Article
Figure 1
Plasma Levels of C-Reactive Protein (Panel A) and Serum Amyloid A Protein (Panel B) in Patients with Stable Angina (Group 1), Patients with Unstable Angina and Levels of C-Reactive Protein <0.3 mg per Deciliter on Admission (Group 2A), and Patients with Unstable Angina and Levels of C-Reactive Protein greater than or equal to 0.3 mg per Deciliter on Admission (Group 2B).Figure 2
Changes in the Median Levels of C-Reactive Protein (Open Circles) and Serum Amyloid A Protein (Solid Circles) and the Mean Level of Cardiac Troponin T (Solid Squares) after Admission in Patients with Unstable Angina and Concentrations of C-Reactive Protein <0.3 mg per Deciliter (Group 2A) Whose Symptoms Were Controlled with Medical Therapy, Two Patients in Group 2A with Increased Values for C-Reactive Protein and Serum Amyloid A Protein and Worsening Symptoms, and Patients with Unstable Angina and Concentrations of C-Reactive Protein greater than or equal to 0.3 mg per Deciliter (Group 2B).Article Activity
- Article
In patients with unstable angina, persistent or worsening symptoms and signs of ischemia despite full medical therapy indicate a poor prognosis1-6. However, at the time of hospital admission, it is not possible to predict whether unstable angina will remit or progress to myocardial infarction, because the causes of instability and the mechanisms underlying its evolution are not known.
A role for inflammation in unstable angina is suggested by histologic studies of unstable coronary plaques,7-10 evidence of the systemic release of thromboxanes and leukotrienes,11-13 and the presence of activated circulating leukocytes14,15. Furthermore, increased concentrations of plasma C-reactive protein, the prototypal acute-phase reactant, have been reported in some patients with unstable angina,16 in patients with coronary artery disease and other types of angina,17 and in 20 percent of patients who have an acute myocardial infarction within six hours after the onset of symptoms, before any elevation of myocardial-enzyme levels in serum18. The acute-phase reactants are very sensitive, although nonspecific, markers of inflammation. However, previous studies of the acute-phase reactants in unstable angina were performed with routine assays for C-reactive protein, which have limited sensitivity.
We undertook a prospective study of patients with severe unstable angina, patients with severe coronary artery disease and chronic stable angina, and patients with a myocardial infarction of less than six hours' duration. We used newly developed, highly sensitive immunoassays for C-reactive protein and serum amyloid A protein, another acute-phase protein19. In addition, we measured cardiac troponin T, a specific marker of myocardial necrosis20.
Methods
Patients
Group 1 comprised 32 outpatients with stable angina that had lasted for more than six months, angiographically confirmed coronary artery disease, and no clinically evident ischemic episodes during the previous week. The group included 26 men and 6 women, with a mean (±SD) age of 58 ±9.4 years. All 32 patients were taking aspirin; in addition, some used oral nitrates, calcium antagonists, and beta-blockers as required.
Group 2 comprised 31 of the 82 patients with severe unstable angina who were hospitalized in our coronary care unit between March 1992 and March 1993. There were 28 men and 3 women, with a mean age of 59.8 ±8.4 years. The criteria for enrollment in group 2 included angina at rest with at least two episodes in the previous 48 hours or one episode lasting more than 20 minutes, ST-segment deviations that were diagnostic of myocardial ischemia during anginal attacks, an episode of chest pain within the previous 24 hours, and no elevation in the serum creatine kinase or lactate dehydrogenase concentration on admission. The symptoms of unstable angina had started 2 to 15 days (mean, 6 ±4) before admission. The criteria for exclusion were an interval of more than 24 hours since the last ischemic episode before hospitalization (28 patients), a myocardial infarction within the previous month (10), an elevated creatine kinase or lactate dehydrogenase level on admission (4), intercurrent inflammatory or neoplastic conditions likely to be associated with an acute-phase response (7), valvular heart disease (1), and a left bundle-branch block invalidating the ST-segment analysis (1). All patients underwent Holter monitoring for the first 24 hours after admission and received various combinations of calcium antagonists, oral nitrates, beta-blockers, and aspirin; intravenous nitrates and heparin were given as required for persistent ischemia. Coronary angiography was performed within five days after admission in 15 patients with refractory angina requiring urgent revascularization; in 8 patients angiography was performed five to nine days after admission, and in 4 it was performed five to seven days after they had had a myocardial infarction.
Group 3 comprised 29 of the 105 patients admitted during the same period with a diagnosis of possible acute myocardial infarction. There were 21 men and 8 women, with a mean age of 60 ±10 years. The criteria for enrollment were admission within 6 hours after the onset of prolonged chest pain, with ST changes typical of infarction and a normal serum creatine kinase level on admission, rising within 8 to 24 hours to a level that was diagnostic of infarction. The criteria for exclusion were admission more than 6 hours after the onset of symptoms (41 patients, 34 of whom had elevated creatine kinase levels on admission), inflammatory or neoplastic disease (21), a left bundle-branch block or atrial fibrillation (13), and a chronic dissecting aortic aneurysm (1).
Study Protocol
Venous blood samples were obtained during a single outpatient visit for patients in group 1, and on admission to the hospital, 6 hours later, daily for three days, and at discharge for patients in groups 2 and 3; in group 2 additional blood samples were obtained every 6 hours for the first 24 hours. Coded plasma samples were stored at -70 °C and analyzed for C-reactive protein, serum amyloid A protein, and cardiac troponin T in a single batch at the end of the study; all decisions regarding the care of the patients were made independently of these measurements. Total creatine kinase levels were determined routinely when the blood samples were obtained. A major coronary event was defined as myocardial infarction or cardiac death; a minor event was defined as urgent coronary angioplasty or bypass grafting because of the failure of medical therapy to control ischemic episodes and, in group 3, postinfarction angina. All patients gave informed consent to participate in the study, and the protocol was approved by the Ethics Committee of the Catholic University of Rome.
Plasma Protein Assays
C-reactive protein was assayed by rate nephelometry (Behring NA latex CRP; Behring Institute, Scoppito, l'Aquila, Italy) and, in samples with less than 0.25 mg of C-reactive protein per deciliter, by an automated monoclonal-antibody, solid-phase, sandwich-type enzyme immunoassay (IMX, Abbott Laboratories, North Chicago), calibrated with the World Health Organization's International Reference Standard for CRP Immunoassay (85/506)21; the range of values detected by the assay is 0.005 to 3.0 mg per deciliter. The median normal value for C-reactive protein is 0.08 mg per deciliter, with 90 percent of normal values <0.3 mg per deciliter and 99 percent <1.0 mg per deciliter22. Serum amyloid A protein was measured by an automated monoclonal-polyclonal-antibody, solid-phase, sandwich-type enzyme immunoassay (Abbott)23. The normal mean (±SD) concentration is 0.37 ±0.36 mg per deciliter; the median value is 0.30 mg per deciliter (range, 0.07 to 2.64), with 82 percent of normal values <0.5 mg per deciliter and 96 percent <1.0 mg per deciliter23. Troponin T was measured by enzyme immunoassay (Boehringer, Mannheim, Germany).
Statistical Analysis
The data on C-reactive protein and serum amyloid A protein, which were not normally distributed, were analyzed with two nonparametric tests: the Mann-Whitney rank-sum test and Spearman's rank correlation coefficient24. The chi-square test was used to compare discrete variables, and unpaired t-tests to compare clinical variables. P values less than 0.05 (two-tailed) were considered to indicate statistical significance.
Results
Patients with Stable Angina
The concentration of C-reactive protein was ≥ 0.3 mg per deciliter in only 4 of the 32 patients (13 percent) with stable angina (group 1) (Figure 1Figure 1
Plasma Levels of C-Reactive Protein (Panel A) and Serum Amyloid A Protein (Panel B) in Patients with Stable Angina (Group 1), Patients with Unstable Angina and Levels of C-Reactive Protein <0.3 mg per Deciliter on Admission (Group 2A), and Patients with Unstable Angina and Levels of C-Reactive Protein greater than or equal to 0.3 mg per Deciliter on Admission (Group 2B).); the median concentration of serum amyloid A protein in these 4 patients was 0.3 mg per deciliter (range, 0.1 to 1.3). In the other 28 patients with stable angina (88 percent), the median concentration of serum amyloid A protein was 0.15 mg per deciliter (range, 0.1 to 0.4). There were no differences in clinical or angiographic characteristics between patients with levels of C-reactive protein ≥ 0.3 mg per deciliter and those with levels <0.3 mg per deciliter. At six months, all four patients in whom C-reactive protein had initially been elevated were still stable.Patients with Unstable Angina
Plasma Protein Levels on Admission
The mean (±SD) concentrations of creatine kinase (80 ±53 IU per liter [range, 20 to 229; reference range, 30 to 230]) and troponin T (0.02 ±0.04 μg per liter [range, 0 to 0.14; reference range, 0 to 0.2]) were normal in all 31 patients with unstable angina (group 2). In contrast, the concentration of C-reactive protein was <0.3 mg per deciliter in only 11 of the 31 patients (35 percent) (group 2A). The plasma C-reactive protein concentration was increased in the other 20 patients (65 percent) (group 2B) (P<0.001 for the comparison with the stable-angina group) (Figure 1). Serum amyloid A protein levels were normal in all but one patient in group 2A and were raised in all the patients in group 2B (Table 1Table 1
Levels of C-Reactive Protein and Serum Amyloid A Protein and Clinical Characteristics in 31 Patients with Unstable Angina.).Clinical Characteristics
There were no differences between groups 2A and 2B with respect to base-line clinical characteristics or treatment (Table 1), and among the 27 patients in whom coronary angiography was performed during the study, the C-reactive protein level was not correlated with the number of diseased vessels, severity or extent of lesions, or number of segments involved25. Age, sex, risk factors, and base-line therapy were similar in the patients with stable angina and those with unstable angina, and there were no significant differences between the two groups in the number of stenotic vessels or the pattern of coronary disease.
Clinical Course in the Hospital
The patients with levels of C-reactive protein <0.3 mg per deciliter on admission to the coronary care unit were discharged sooner (mean, 5.4 ±3 days) than those with elevated levels (mean, 9.8 ±7 days; P = 0.04). Furthermore, among the patients with normal levels of C-reactive protein on admission, there were only six ischemic episodes, five of which were clinically silent, in the first 24 hours of Holter monitoring. There were few episodes of recurrent angina and no major coronary events (Table 2Table 2
Recurrent Angina, Ischemic Episodes, Myocardial Revascularization, and Coronary Events in Patients with Unstable Angina.). Only two patients required coronary-artery bypass grafting, at day 9 in the first patient and at day 5 in the second, and both had an acute-phase response during the first four days of monitoring, with the C-reactive protein level increasing from 0.25 to 1.9 mg per deciliter in the first patient and from 0.27 to 3.2 mg per deciliter in the second, and the serum amyloid A protein level increasing from 0.20 to 1.53 mg per deciliter in the first patient and from 0.28 to 3.0 mg per deciliter in the second. Despite therapy that included intravenous nitrates and heparin, both patients had recurrent episodes of angina at rest (the first had five episodes, and the second had three), requiring urgent surgical revascularization. Of the 15 blood samples obtained from these two patients during the first four days of the study, 5 had levels of C-reactive protein and serum amyloid A protein above the normal range, but none had abnormal levels of creatine kinase or troponin T (Figure 2Figure 2Changes in the Median Levels of C-Reactive Protein (Open Circles) and Serum Amyloid A Protein (Solid Circles) and the Mean Level of Cardiac Troponin T (Solid Squares) after Admission in Patients with Unstable Angina and Concentrations of C-Reactive Protein <0.3 mg per Deciliter (Group 2A) Whose Symptoms Were Controlled with Medical Therapy, Two Patients in Group 2A with Increased Values for C-Reactive Protein and Serum Amyloid A Protein and Worsening Symptoms, and Patients with Unstable Angina and Concentrations of C-Reactive Protein greater than or equal to 0.3 mg per Deciliter (Group 2B).). The levels of C-reactive protein and serum amyloid A protein remained normal in the other nine patients until discharge; these patients had few episodes of ischemia during hospitalization (mean, 1.4 ±2.3), and they did not require angioplasty or bypass surgery.Among the patients with C-reactive protein levels ≥ 0.3 mg per deciliter on admission, there were 24 ischemic episodes, 11 of which were clinically silent, in the first 24 hours of Holter monitoring. The duration of electrocardiographic signs of ischemia was significantly longer in these patients, and the number of episodes of recurrent angina significantly higher, than in the group with normal levels of C-reactive protein on admission (Table 2). Moreover, six of the patients with elevated levels of C-reactive protein had major coronary events: five had a myocardial infarction within 10 days after admission, and one of the five, who had a large infarct, died of congestive heart failure within 1 month; one other patient died after emergency bypass surgery. All six of these patients had increased levels of C-reactive protein (median, 2.72 mg per deciliter; range, 1.09 to 8.25) and serum amyloid A protein (median, 6.53 mg per deciliter; range, 2.7 to 26.42) on admission. Only two patients with levels of C-reactive protein >1.0 mg per deciliter and levels of serum amyloid A protein >2.7 mg per deciliter did not have major coronary events; however, both required urgent coronary angioplasty. Indeed, 12 of 20 patients had refractory unstable angina requiring urgent bypass surgery or angioplasty (Table 2 and Figure 1).
In 8 of 20 patients the values for C-reactive protein and serum amyloid A protein doubled between 24 and 72 hours after admission, in the absence of elevated levels of cardiac troponin T or any other evidence of myocardial necrosis. Three of these eight patients had major coronary events, and another five required urgent angioplasty (in three patients) or bypass surgery (in two) to control symptoms in spite of therapy with intravenous heparin and, in one patient, thrombolytic treatment.
There were no increases in creatine kinase or cardiac troponin T levels in any of the blood samples obtained during the observation period except those obtained after the development of electrocardiographically confirmed myocardial infarction in five patients with raised levels of C-reactive protein on admission. Therefore, the raised levels of C-reactive protein and serum amyloid A protein in our patients cannot be attributed to the presence of myocardial necrosis.
The sensitivity of a C-reactive protein level ≥ 0.3 mg per deciliter on admission as a marker for subsequent cardiac events (myocardial infarction or death), urgent angioplasty, or bypass grafting was 90 percent, the specificity was 82 percent, and the positive predictive value was 90 percent. The sensitivity, specificity, and positive predictive value changed only slightly when the level of serum amyloid A protein was used as a prognostic marker on admission (90, 73, and 86 percent, respectively). When any increase in the level of C-reactive protein or serum amyloid A protein was considered at any time during the study, the sensitivity rose to 100 percent with a specificity of 82 percent and a positive predictive value of 90 percent.
Patients with Myocardial Infarction
Plasma Protein Levels on Admission
Troponin T was undetectable and creatine kinase values were normal (mean, 136.2 ±77; range, 21 to 228; reference range, 30 to 230) in all 29 patients with myocardial infarction (group 3). In contrast, the levels of C-reactive protein and serum amyloid A protein at admission were <0.3 mg per deciliter in only seven of the patients (24 percent) (group 3A) (Table 3Table 3
Levels of C-Reactive Protein and Serum Amyloid A Protein and Clinical Characteristics in 29 Patients with Myocardial Infarction.). None of these 7 had had unstable angina before admission, as compared with 14 of the 22 patients (64 percent) with elevated levels of C-reactive protein on admission (P = 0.01) (Table 3). Two patients with normal values for C-reactive protein on admission had had chronic stable angina, but in the other five, the myocardial infarction was unheralded. In the group of 22 patients with elevated C-reactive protein levels on admission (group 3B), 1 had a history of chronic stable angina, and 7 presented with unheralded myocardial infarction (Table 3); the other 14 patients had all had their last episode of unstable angina within 48 hours before the myocardial infarction. In the group as a whole, there was no correlation between the time from the onset of symptoms of myocardial infarction (mean, 3.3 ±1.6 hours) and the C-reactive protein or serum amyloid A protein level on admission.Follow-up in Hospital
The values for the acute-phase proteins on admission were also related to the subsequent course of disease. Angina after myocardial infarction occurred in only one of seven patients with normal levels of C-reactive protein on admission, and none of these patients had recurrent infarction in the hospital or required revascularization. In contrast, 14 of the 22 patients (64 percent) admitted with elevated C-reactive protein levels had postinfarction angina, 6 of whom required coronary revascularization, and 3 patients had recurrent infarction while in the hospital, although none died (Table 4Table 4
Postinfarction Angina and Coronary Events in Patients with Myocardial Infarction. and Figure 3Figure 3
Concentrations of C-Reactive Protein (Panel A) and Serum Amyloid A Protein (Panel B) in Patients Admitted with Myocardial Infarction, with (Open Squares) or without (Open Circles) a History of Unstable Angina.).The patients with a history of unstable angina before myocardial infarction generally had higher values for acute-phase proteins (median level of C-reactive protein, 0.84 mg per deciliter; range, 0.39 to 6.98; median level of serum amyloid A protein, 1.74 mg per deciliter; range, 0.32 to 28.24) than those in whom the infarction was unheralded or preceded by stable angina (median level of C-reactive protein, 0.31 mg per deciliter; range, 0.24 to 0.89; P<0.001; median level of serum amyloid A protein, 0.34 mg per deciliter; range, 0.07 to 0.79; P<0.001). All patients with a value for either C-reactive protein (four patients) or serum amyloid A protein (nine patients) >1.0 mg per deciliter on admission had had unstable angina before the myocardial infarction.
The typical acute-phase response of C-reactive protein and serum amyloid A protein after infarction was observed. The median peak value for C-reactive protein was 5.04 mg per deciliter (range, 0.67 to 15.8) at a mean of 45.7 ±20.2 hours, and the median peak value for serum amyloid A protein was 20.3 mg per deciliter (range, 0.66 to 114.0) at a mean of 43.3 ±24 hours. Creatine kinase levels rose to 1628 IU per liter (range, 316 to 5044). There was no correlation between the peak creatine kinase value and the admission or peak value for C-reactive protein or serum amyloid A protein. Peak values for C-reactive protein in the patients with confirmed infarction (Figure 3) overlapped those in the patients with unstable angina and C-reactive protein values ≥ 0.3 mg per deciliter on admission (group 2B), but the latter patients had no increase in creatine kinase or troponin T levels and no signs of myocardial infarction (Figure 1).
When all three groups of patients (those with stable angina, those with unstable angina, and those with myocardial infarction) were combined, there was, as expected, a close correlation between the concentrations of C-reactive protein and serum amyloid A protein (Figure 4Figure 4
Correlation between the Concentrations of C-Reactive Protein and Serum Amyloid A Protein in the Combined Groups with Unstable Angina and Myocardial Infarction.).Discussion
Previous studies have reported elevated values for acute-phase proteins in patients with unstable angina16,26,27 and in those who have had a myocardial infarction,26-31 but these studies did not investigate the prognostic importance of the elevated values, nor did they exclude the possibility that myocardial-cell damage causes the acute-phase response. The results of our study confirm the observation that the plasma concentration of C-reactive protein is elevated in the majority of patients with unstable angina, and we also found that C-reactive protein is elevated at the time of hospital admission in all patients with myocardial infarction and a history of unstable angina. Creatine kinase and troponin T levels were within normal limits in all these patients, indicating that the C-reactive protein response is not induced by myocardial necrosis, which is known to be a potent stimulus of acute-phase reactants.
A value for C-reactive protein ≥ 0.3 mg per deciliter on admission had a sensitivity of 90 percent and a specificity of 82 percent for predicting subsequent cardiac events (cardiac death, myocardial infarction, or the urgent need for coronary revascularization). The sensitivity increased to 100 percent in the patients with a value for C-reactive protein >1.0 mg per deciliter on admission and in those who had any rise in the C-reactive protein level during the study. These findings are consistent with the increased values for C-reactive protein in the patients with myocardial infarction preceded by unstable angina.
The results were similar with measurements of serum amyloid A protein, another extremely sensitive acute-phase reactant. Indeed, serum amyloid A protein may be more useful in routine practice than C-reactive protein, because it has an even wider dynamic range and because none of the commercially available automated assays for C-reactive protein are sufficiently precise in the low range, as compared with the assay for serum amyloid A protein used in this study. Measurement of both serum amyloid A protein and C-reactive protein slightly increased the prognostic precision, but for clinical purposes the information provided by each alone is the same. However, it is essential to recognize the requirement for assays of C-reactive protein and serum amyloid A protein with a suitably high sensitivity, encompassing the normal range of values.
The acute-phase response of C-reactive protein and serum amyloid A protein is a nonspecific phenomenon reflecting cytokine-mediated hepatic production triggered by most forms of inflammation, infection, and tissue injury. Our patients were carefully selected to eliminate intercurrent disorders likely to be associated with an acute-phase response, and similar attention to intercurrent processes will be essential for the practical application of our findings.
An association has been reported between prognosis and the persistence of pain at rest or episodes of silent ischemia during Holter monitoring1-6. We also found that the number and length of recurrent ischemic episodes in patients with favorable outcomes differed significantly from the number and length of episodes in patients with unfavorable outcomes, which confirms the results of previous studies,1-6 but the sensitivity and specificity associated with the use of recurrent ischemia as a prognostic marker were lower than those associated with the use of C-reactive protein measurements. A recent study reported elevated levels of cardiac troponin T in 39 percent of patients with angina at rest, which were significantly related to prognosis, but the report contained no information on the number or duration of ischemic episodes20. The absence of elevated values of cardiac troponin T in our patients may reflect the absence of long-lasting ischemic episodes in our study group.
Our results, together with the evidence of an inflammatory component documented in previous studies,7-11,13-17 have important pathophysiologic implications, and the predictive correlation between the level of C-reactive protein and the clinical outcome links the acute-phase response with pathogenetic events. However, it is not known whether the elevated levels of acute-phase proteins are related to the type of inflammatory stimuli or to the intensity of the individual response32. It is also not known whether the stimuli triggering the production of acute-phase proteins arise from the heart15 or other parts of the body14. Ischemia-induced endothelial damage, oxidized low-density lipoprotein,33 immune complexes, and reactivation of dormant cytomegalovirus or chlamydia infection34,35 are all potential causes of vascular injury and an acute-phase response. In addition to their practical clinical importance, the present observations point to new avenues of investigation into the causes of unstable angina and myocardial infarction.
Supported by a grant from the Centro Ricerche Coronariche.
We are indebted to Professors A. Menini and G. Satta for help with laboratory investigations, to Dr. G. Caligiuri and the nurses of the coronary care unit at Policlinico Gemelli for their assistance, and to Ms. B. Sontrop for assistance in the preparation of the manuscript.
Source Information
From the Istituto di Cardiologia (G.L., L.M.B., A.G.R., A.M.) and Istituto di Microbiologia (R.L.G.), Universita Cattolica del Sacro Cuore, Rome; and the Immunological Medicine Unit, Department of Medicine, Royal Postgraduate Medical School, Hammersmith Hospital, London (J.R.G., M.B.P.).
Address reprint requests to Dr. Liuzzo at the Istituto di Cardiologia, Universita Cattolica del Sacro Cuore, Largo Agostino Gemelli 8, 00168, Rome, Italy.
- References
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