Original Article
The Erythrocyte Sedimentation Rate in Congestive Heart Failure
N Engl J Med 1991; 324:353-358February 7, 1991
- Abstract
Background and Methods.
Physicians have long believed that the erythrocyte sedimentation rate is low in patients with congestive heart failure, but this concept is based on a misinterpretation of the results in a single report published in 1936. To reevaluate this concept in the modern era, we measured the sedimentation rate in 242 patients who were referred for treatment of chronic heart failure.
Results.
The sedimentation rate was low (less than 5 mm per hour) in only 24 patients percent) but was increased (above 25 mm per hour) in 50 percent. Patients with low or normal sedimentation rates (≤25 mm per hour) had more severe hemodynamic abnormalities than patients with elevated rates: lower cardiac index (mean ±SEM, 1.7±0.1 vs. ±0.1 liters per minute per square meter of body-surface area) and higher mean right atrial pressure (mean ±SEM, 12±1 vs. 9±1 mm Hg) (both P<0.0001). New York Heart Association functional class IV symptoms were present in 66 percent of the patients with a low or normal sedimentation rate, as compared with 42 percent of those with elevated rates (P<0.0001). After one to three months of therapy, patients whose sedimentation rates decreased showed little hemodynamic or clinical response to treatment, whereas both cardiac performance and functional status improved in patients whose rates increased (P<0.02 for the comparison between groups). The sedimentation rate was correlated with the plasma fibrinogen level (r = 0.64, P = 0.0025), and changes in the sedimentation rate during treatment were correlated inversely with changes in mean right atrial pressure (r =-0.57, P = 0.0002). During long-term follow-up, patients with low or normal sedimentation rates had a worse one-year survival than patients with elevated rates (41 vs. 66 percent, P = 0.01
Conclusions.
These data indicate that the erythrocyte sedimentation rate is correlated with the severity of illness in patients with chronic heart failure. Because of its lack of discriminatory power, however, the test is of limited value in the clinical management of this disorder.
Media in This Article
Figure 1
Distribution of Values for the Erythrocyte Sedimentation Rate in All 242 Patients with Chronic Heart Failure. The values ranged from 0 to 122 mm per hour (mean, 32; median, 25).Figure 2
Relation of the Erythrocyte Sedimentation Rate to the Plasma Fibringen Level in 20 Patients with Chronic Heart Failure.Article Activity
- Article
For more than 50 years, physicians have been taught that the erythrocyte sedimentation rate is low in patients with congestive heart failure.1 This belief, however, stems primarily from observations published in a single report by Paul Wood in 1936.2 He observed a striking retardation of the sedimentation rate in patients presenting with acute pulmonary congestion and peripheral edema followed by an acceleration of the rate when the symptoms of heart failure subsided after treatment with diuretics. Interestingly, subsequent reports (published in the 1950s and 1960s) failed to observe any characteristic changes in the sedimentation rate in this disorder.3-6 The distribution of values in patients with heart failure did not differ from that in patients with heart disease but without evidence of cardiac decompensation,7 and there was no consistent relation between changes in the rate and the clinical course of the disease.3-6 These dissenting reports received little attention, however. Consequently, the observations of Wood have remained an unchallenged (and untested) part of medical folklore for the past five decades.
Regardless of the validity of Wood's original paper, the observations made by physicians to 50 years ago may no longer be relevant to patients with heart failure treated in the 1990s. Most of the patients evaluated in the 1930s through the 1960s presented with acute heart failure,2-7 and the deterioration in their condition was frequently related to an associated myocardial infarction or pulmonary infection,4-7 which was often undiagnosed by the treating physician.4,8,9 Many of the patients had fever, which was mistakenly attributed to the heart failure itself when a source of infection could not be identified.4 Other patients had evidence of active rheumatic carditis or had heart failure due to cor pulmonale (often associated with polycythemia).2-7 These associated disorders can influence the sedimentation rate directly and thus complicate interpretation of the findings of these reports. Furthermore, the syndrome of heart failure in these early studies was poorly characterized, since modern invasive and noninvasive techniques for assessing the pathophysiologic features and severity of heart failure had not been developed. Consequently, it was not possible for early investigators to explain how the hemodynamic abnormalities of heart failure could alter the rate of erythrocyte sedimentation. Finally, symptomatic improvement in the early reports was produced primarily by the vigorous use of diuretics, but because these drugs can cause hemoconcentration, they may alter the sedimentation rate independently of their effects on the clinical course of the disease.1 In view of these difficulties in interpretation, it seemed appropriate to reevaluate the importance of the erythrocyte sedimentation rate in a large and well-characterized group of patients with congestive heart failure who were being treated in the vasodilator era.
Methods
Patient Population
All patients had had dyspnea and fatigue at rest or on minimal exertion (New York Heart Association functional class III or IV) for at least six months, despite optimal therapy with digoxin and diuretics; the doses of diuretics had been titrated previously so that there was no evidence of edema on physical examination. All patients were evaluated during a period of clinical stability; patients were excluded if they had had an acute myocardial infarction within eight weeks of the study or an acute exacerbation of heart failure within two weeks or had any evidence of a neoplastic, collagen vascular, infectious, inflammatory, or febrile disorder. No patient had heart failure due to cor pulmonale or acute myocarditis or had polycythemia.
Study Protocol
All base-line measurements were carried out during a five-day inhospital evaluation period during which doses of digoxin and diuretics were held constant and no vasodilator drugs were administered. During this time, blood was collected from all patients for the measurement of the following: the erythrocyte sedimentation rate (by the modified Westergren method10) (normal range, 5 to 25 mm per hour); blood urea nitrogen and serum creatinine; the hemoglobin concentration; serum bilirubin, aspartate and alanine aminotransferases, and alkaline phosphatase; and serum protein, serum albumin, and prothrombin time. In addition, plasma fibrinogen was measured in 20 patients, plasma renin activity (by radioimmunoassay11) in 151 patients, plasma norepinephrine (by radioenzymatic assay12) in 76 patients, and the left ventricular ejection fraction (by radionuclide ventriculography) in 110 patients. At the end of the five-day observation period, all patients underwent catheterization of the right side of the heart and arterial cannulation for the measurement of intracardiac and systemic pressures, respectively, with the use of procedures that have been described previously.13
After base-line hemodynamic measurements were completed, long-term treatment with approved or investigational vasodilator or positive inotropic agents was begun. The selection of a drug for an individual patient was determined by the protocols that were active at the time each patient was evaluated; treatment was not randomly assigned in this study. Long-term therapy consisted of direct-acting vasodilators (hydralazine, isosorbide dinitrate, flosequinan, or fenoldopam) in 106 patients, converting-enzyme inhibitors (captopril or enalapril) in 123 patients, and the phosphodiesterase inhibitor amrinone in 3 patients. Ten patients received no new treatment.
The sedimentation rate was remeasured in 35 patients who underwent a second right-sided heart catheterization after one to three months of therapy, during which time the doses of digoxin and diuretics were unchanged. All hematologic, biochemical, and hemodynamic variables that had been assessed during the base-line period were reevaluated at this time. The functional status of each patient was assessed by a physician who had no knowledge of the pretreatment or post-treatment values of the sedimentation rate.
Statistical Analysis
Long-term survival was assessed from the day of the first catheterization to the day of death or to the most recent follow-up visit, with use of methods that we have described previously.14 Eight patients were lost to follow-up; their survival data were censored after the date of their last contact. Cumulative survival curves were constructed according to Kaplan–Meier survivorship methods,15 and differences between the survival curves were tested for significance by the Wilcoxon—Breslow method.16 All pretreatment variables listed in Table 1Table 1
Hemodynamic and Clinical Characteristics of Patients with Heart Failure, Grouped According to the Pretreatment Erythrocyte Sedimentation Rate (excluding the sedimentation rate) were entered into a stepwise Cox proportional-hazards model (Biomedical Computer Programs, BMDP-2L) to assess their potential association with survival; the sedimentation rate was then added to the model to assess its ability to provide incremental prognostic information.Patients were divided into two equal groups on the basis of the median value for the sedimentation rate for the entire cohort; this value (25 mm per hour) coincided with the upper limit of normal for our study patients.17,18 Qualitative and quantitative comparisons of the two groups with respect to 24 pretreatment hemodynamic, clinical, and biochemical variables were performed with the chi-square statistic and the t-test (two-tailed) for independent variables, respectively. Because of the multiplicity of comparisons, a P value of less than 0.05/24, or 0.0021 Bonferroni correction), was used to indicate statistical significance. In the patients who were evaluated a second time, the significance of observed relations between changes in the sedimentation rate and changes in 15 hemodynamic and biochemical variables was tested by linear regression methods; a P value of less than 0.05/15, or 0.0033 (Bonferroni correction), was used to indicate statistical significance. Among these 35 patients, comparisons were then carried out between two subgroups: those with an increase and those with a decrease in the sedimentation rate of at least 5 mm per hour (which represented a change more than 2 SD larger than the spontaneous change in the rate observed over time in normal subjects). Group data are expressed as means ±SEM.
Results
The erythrocyte sedimentation rate in our patients ranged from 0 to 122 mm per hour (median, 25) (Fig. 1Figure 1
Distribution of Values for the Erythrocyte Sedimentation Rate in All 242 Patients with Chronic Heart Failure. The values ranged from 0 to 122 mm per hour (mean, 32; median, 25).). The rate of sedimentation was low (<5 mm per hour) in only 24 patients (10 percent), whereas in 50 percent the sedimentation rate was more than 25 mm per hour (the upper limit of normal). When factors known to influence the sedimentation rate were analyzed, values for the rate varied linearly and directly with the plasma fibrinogen level (r = 0.64, P = 0.0025), but not with the serum albumin or globulin level (Fig. 2Figure 2Relation of the Erythrocyte Sedimentation Rate to the Plasma Fibringen Level in 20 Patients with Chronic Heart Failure. and Table 1). In addition, the hemoglobin concentration was reduced in patients with the highest sedimentation rate (P<0.0001) (Table 1).The 121 patients with sedimentation rates
25 mm per hour (rates below the median value) were similar to the 121 patients with higher rates with respect to age and sex, cause and treatment of heart failure, renal function, and hormonal measurements (Table 1). Patients with low sedimentation rates had more severe symptoms than patients with high rates class IV symptoms were present in 66 percent and 42 percent, respectively; P<0.0001). Values for cardiac index were lower in patients with slower sedimentation (P<0.0001), but noninvasive and invasive measures of left ventricular function (left ventricular ejection fraction and pulmonary wedge pressure) were similar in the two groups. Hence, the low cardiac index in patients with a low sedimentation rate was related to their more advanced right- sided heart failure (as reflected by higher mean right atrial pressures and serum bilirubin levels; both P<0.0001). When a multiple regression analysis was carried out with the five variables in Table 1 that were significantly different between groups, hemoglobin, functional class, and mean right atrial pressure were independent correlates of the sedimentation rate.When they were considered as a group, there was no significant change in the sedimentation rate after one to three months of therapy in the 35 patients who had a second hemodynamic assessment. However, the 19 patients in whom the sedimentation rate increased by at least 5 mm per hour had more marked hemodynamic and clinical benefits than the 11 patients in whom the rate decreased by 5 mm per hour or more. An improvement in functional class was seen in 15 of the 19 patients whose sedimentation rate increased but in only 3 of the 11 patients whose rate declined vs. 27 percent, P = 0.017). Patients whose sedimentation rates increased had larger increases in cardiac index (P = 0.01) and larger decreases in pulmonary wedge pressure (P = 0.002), mean arterial pressure (P = 0.02), mean right atrial pressure P = 0.002), and systemic vascular resistance (P = 0.01) than patients whose rates decreased (Table 2Table 2
Hemodynamic Responses to Vasodilator Therapy in Patients Grouped According to the Change in Sedimentation Rate during Treatment). When all 35 patients were considered, changes in the sedimentation rate were linearly correlated with changes in mean right atrial pressure (P = 0.0002) (Fig. 3Figure 3
Relation between the Change in the Erythrocyte Sedimentation Rate and the Change in Mean Right Atrial Pressure in 35 Patients Who underwent a Second Hemodynamic and Biochemical Evaluation after One to Three Months of Treatment with Vasodilator Drugs.), pulmonary wedge pressure (P = body weight (P = 0.01), and serum bilirubin level (P = 0.01) — specifically, the rate increased as intracardiac pressures, weight, and bilirubin decreased — but not with changes in hemoglobin, globulin, or albumin.During long-term follow-up, patients with a higher sedimentation rate fared significantly better than those with a lower rate (median survival, 523 vs. 367 days) (Fig. 4Figure 4
Kaplan–Meier Analysis Showing Cumulative Rates of Survival in Patients with Chronic Heart Failure Stratified According to Erythrocyte Sedimentation Rate (ESR) at the Start of the Study. Patients with an elevated sedimentation rate (>25 mm per hours) had a significantly more favorable outcome than patients with a low or normal rate (P = 0.01).). The one-year and two-year survival rates were 66 percent and 41 percent, respectively, in patients with a higher sedimentation rate, but only 51 percent and 29 percent in those with lower values (P = 0.01 for the comparison between groups). When all the variables listed in Table 1 were entered into a Cox analysis to evaluate their potential association with survival, complete data were available for only 36 patients (since ejection fraction, plasma renin activity, and plasma norepinephrine were not measured in all patients); however, the three variables for which data were available only for these 36 patients were not correlated with survival in that small subgroup. When these three variables were excluded from the analysis, four variables were found to be independent correlates of survival: pulmonary wedge pressure (Ζ2 = serum bilirubin level (Ζ2 = 12.01), serum creatinine concentration (Ζ2 = and age (Ζ2 = 5.98). When only these four variables were considered in the Cox model, the addition of the erythrocyte sedimentation rate provided independent, incremental prognostic information (Ζ2 = 6.08, P<0.05).Discussion
The findings of the present study do not support the classic teaching1 that the erythrocyte sedimentation rate is characteristically low in patients with congestive heart failure. The rate of sedimentation was less than 5 mm per hour in only 10 percent of our patients, whereas half of our patients had a rate of more than 25 mm per hour (the upper limit of normal for our study patients; mean age, 64 years).17,18 At first glance, this conclusion would appear to differ importantly from that reached by Wood2 more than 50 years ago. Contrary to popular belief, however, Wood did not conclude that the sedimentation rate was low in chronic heart failure, but that the rate declined in patients who had worsening congestive symptoms and that it increased in patients who responded favorably to treatment. In fact, most of Wood's patients had an elevated sedimentation rate during the chronic phase of their illness. The observations of Wood and subsequent investigators3-7,19 should be interpreted cautiously, however, since these studies did not include objective hemodynamic measurements or exclude patients who had associated disorders that could alter the rate of erythrocyte sedimentation.
Our data provide objective evidence (in a well-characterized group of patients with heart failure not complicated by inflammatory disorders) that depression of the sedimentation rate reflects a state of severe cardiac decompensation. As compared with patients with rapid sedimentation, the patients who had a low or normal sedimentation rate in our study had more advanced heart failure, as indicated by the greater severity of their symptoms and hemodynamic abnormalities lower cardiac output and higher central venous pressures) and their more unfavorable long-term survival rate. Further- more, changes in the sedimentation rate closely paralleled changes in the clinical and hemodynamic status of these patients. Patients whose sedimentation rate increased generally improved hemodynamically and symptomatically, whereas the rate declined further in patients who did not respond favorably to vasodilator therapy. These data indicate that the severity (rather than the presence) of heart failure is the chief determinant of the rapidity of erythrocyte sedimentation in patients with left ventricular dysfunction.
Although the sedimentation rate was related to the severity of heart failure, the most important hemodynamic correlate of the sedimentation rate was not left ventricular function but mean right atrial pressure. Not only was the sedimentation rate correlated inversely with the level of right atrial pressure before treatment, but changes in rate were correlated inversely with changes in right atrial pressure during treatment. This correlation of the sedimentation rate with right atrial pressure may explain why both we and Wood2 noted an increase in the sedimentation rate in patients who had a diuresis after the institution of effective therapy. Conversely, the sedimentation rate was depressed in our patients who had evidence of right-sided heart failure and hepatic congestion (as shown by an increased serum bilirubin level), despite optimal therapy with digoxin and diuretics. It is noteworthy that a relation between the sedimentation rate and mean right atrial pressure was observed by Parry 30 years ago,6 but was regarded by the author as a fortuitous association.
How could an elevation of mean right atrial pressure lead to a reduction in the sedimentation rate? Fibrinogen appears to be the primary determinant of the sedimentation rate in patients with heart failure, as it is in many inflammatory disorders.20-22 The sedimentation rate varied directly with the plasma fibrinogen level in our patients, and changes in fibrinogen level have been shown to correlate closely with changes in the sedimentation rate in this disorder.21 Interestingly, many patients with chronic heart failure due to left ventricular dysfunction have chronically elevated levels of fibrinogen (>4 g per liter) (Fig. 2),19,23 and thus have an increased sedimentation rate (Fig. 1).3,5-7 This finding may be related to their advanced age24,25 or the high prevalence of coronary artery disease,26,27 systemic hypertension,28 and diabetes mellitus29 in these patients. However, during periods of acute decompensation or when the clinical syndrome of right-sided heart failure ensues in patients with long-standing left ventricular failure, right atrial pressure rises and hepatic congestion develops. The associated volume expansion could act to dilute the concentration of fibrinogen and thus reduce the sedimentation rate.23 Alternatively, any increase in intrahepatic sinusoidal pressure (due to increased right atrial pressure) might impair the formation or accelerate the degradation of fibrinogen.1,2 If this were to occur, both the plasma fibrinogen level and the sedimentation rate would decline (possibly into the normal or low range), only to rise again after the right atrial pressure was lowered by effective treatment.19
It should be noted that the sedimentation rate can also be accelerated if the concentration of macromolecules relative to that of erythrocytes is increased by lowering the hematocrit.22,30 Although the hematocrit was lower in our patients who had a high sedimentation rate than in those with a lower rate, it seems unlikely that the hematocrit was a major determinant of the rate of erythrocyte sedimentation in the patients in our study, since we would expect patients who had a diuresis after vasodilator therapy to have hemoconcentration,23 and thus a decrease in the sedimentation rate. Yet the sedimentation rate increased in these patients, and there was no relation between changes in hematocrit and changes in the rate of sedimentation in our study.
In conclusion, our study, carried out 50 years after the original report by Wood,2 suggests that the erythrocyte sedimentation rate correlates with the severity of disease in patients with chronic heart failure. The rate reflects dynamic changes in right ventricular filling pressure, which is an important determinant of the functional capacity and long-term clinical outcome of patients with left ventricular dysfunction.31-33 As compared with the bedside estimation of jugular venous pressure, measurement of the sedimentation rate can be more precise and can more reliably be used to evaluate changes in mean right atrial pressure, especially when central venous pressures are very low or very high. Unfortunately, the test is readily affected by many clinical conditions (such as infection) that occur frequently in patients with heart failure; this lack of discriminatory power greatly limits the value of the test in the routine management of this disorder.
Supported by grants (R01-HL-25055, K04-HL-01229, T32-HL-07347, and M01-RR-00071) from the National Institutes of Health. Dr. Packer is the recipient of a Research Career Development Award from the National Heart, Lung, and Blood Institute.
We are indebted to Ms. Norma Medina and Ms. Madeline Yushak for performing the hemodynamic measurements and caring for the patients in this study, and to Ms. Jonine Bernstein for expert statistical analysis.
Source Information
From the Center for Heart Failure Research, Division of Cardiology, Department of Medicine, Mount Sinai School of Medicine, New York. Address reprint requests to Dr. Packer at the Division of Cardiology, Mount Sinai Medical Center, 1 Gustave Levy Pl., New York, NY 10029.
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Donald S Silverberg, Dov Wexler, David Sheps, Miriam Blum, Gad Keren, Ron Baruch, Doron Schwartz, Tatyana Yachnin, Shoshana Steinbruch, Itzhak Shapira, Shlomo Laniado, Adrian Iaina. (2001) The effect of correction of mild anemia in severe, resistant congestive heart failure using subcutaneous erythropoietin and intravenous iron: a randomized controlled study. Journal of the American College of Cardiology 37:7, 1775-1780
CrossRef8
Rakesh Sharma, Mathias Rauchhaus, Piotr P Ponikowski, Susan Varney, Philip A Poole-Wilson, Douglas L Mann, Andrew J.S Coats, Stefan D Anker. (2000) The relationship of the erythrocyte sedimentation rate to inflammatory cytokines and survival in patients with chronic heart failure treated with angiotensin-converting enzyme inhibitors. Journal of the American College of Cardiology 36:2, 523-528
CrossRef9
Donald S Silverberg, Dov Wexler, Miriam Blum, Gad Keren, David Sheps, Eyal Leibovitch, David Brosh, Shlomo Laniado, Doron Schwartz, Tatyana Yachnin, Itzhak Shapira, Dov Gavish, Ron Baruch, Bella Koifman, Carl Kaplan, Shoshana Steinbruch, Adrian Iaina. (2000) The use of subcutaneous erythropoietin and intravenous iron for the treatment of the anemia of severe, resistant congestive heart failure improves cardiac and renal function and functional cardiac class, and markedly reduces hospitalizations. Journal of the American College of Cardiology 35:7, 1737-1744
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