Original Article
Pain in Sickle Cell Disease — Rates and Risk Factors
N Engl J Med 1991; 325:11-16July 4, 1991
- Abstract
- Abstract
Background and Methods.
Acute episodes of pain are the principal symptom of sickle cell disease, but little is known about the epidemiologic features of these episodes or risk factors for them, nor is it known whether patients with high rates of such episodes die prematurely. We prospectively studied the natural history of sickle cell disease in 3578 patients ranging from newborns to persons up to 66 years old who were followed at clinical centers across the United States.
Results.
There were 12,290 episodes of pain in 18,356 patient-years. The average rate was 0.8 episode per patient-year in sickle cell anemia, 1.0 episode per patient-year in sickle β0-thalassemia, and 0.4 episode per patient-year in hemoglobin SC disease and sickle β+-thalassemia. The rate varied widely within each of these four groups — e.g., 39 percent of patients with sickle cell anemia had no episodes of pain, and 1 percent had more than six episodes per year. The 5.2 percent of patients with 3 to 10 episodes per year had 32.9 percent of all episodes. Among patients with sickle cell anemia who were more than 20 years old, those with high rates of pain episodes tended to die earlier than those with low rates. High rates were associated with a high hematocrit and low fetal hemoglobin levels. α-Thalassemia had no effect on pain apart from its association with an increased hematocrit.
Conclusions.
The "pain rate" (episodes per year) is a measure of clinical severity and correlates with early death in patients with sickle cell anemia over the age of 20. Even when the fetal hemoglobin level is low, one can predict that small increments in the level may have an ameliorating effect on the pain rate and may ultimately improve survival. This outcome is particularly encouraging to investigators studying hydroxyurea and other treatments designed to increase the fetal hemoglobin level. (N Engl J Med 1991; 325:11–6.)
Media in This Article
Figure 1
Distribution of Pain Rates among Patients with Sickle Syndromes.Figure 2
Age-Specific Pain Rates (Episodes per Patient-Year) among Male (Dashed Line) and Female (Solid Line) Patients with Sickle Cell Anemia.Article Activity
- Article
PERIODIC, self-limited episodes of excruciating musculoskeletal pain punctuate the lives of patients with sickle cell disease. Often referred to as "crises," these episodes are the principal cause of morbidity among these patients. Although Western observers named sickle cell anemia for its curious microscopical morphologic features, African cultures have named it for its painful episodes. In the Ga language of Ghana, for example, the disease is known as chwechweechwe —"relentless, repetitive chewing." 1 Despite the obvious importance of this clinical syndrome, we know little about its epidemiologic characteristics. Here we report the findings of the National Heart, Lung and Blood Institute's Cooperative Study of Sickle Cell Disease, in which we sought to answer questions frequently asked by patients, clinicians, and investigators: What is the incidence of the episodes of pain, what are the associated risk factors, and are patients with high rates of pain at risk for early death?
Methods
Study Population
The design of the study has been described elsewhere.2 , 3 The present analysis includes 3578 patients (Table 1Table 1
Summary of Inclusions and Exclusions from the Study Analysis among 4082 Patients.*) ranging at enrollment from newborns to persons up to 66 years old. Patients were enrolled by 23 clinical centers across the continental United States, with a broad geographic and urban—rural distribution of subjects. They were followed between 1979 and 1988 (patients entering after May 31, 1986, were excluded from this analysis); the retention rate was 74.3 percent at the end of follow-up (67.7 percent of the patients were under active study, and 6.6 percent had died). Diagnoses were assigned at the Centers for Disease Control on the basis of hemoglobin electrophoresis — i.e., a diagnosis of sickle cell anemia, sickle β0-thalassemia, sickle β+-thalassemia, or hemoglobin SC disease. Patients without diagnoses were excluded from analysis. Alpha-gene mapping4 , 5 was done by Stephen H. Embury at the University of California at San Francisco. Consent was obtained from the patients or their parents or legal guardians.Base-Line and Steady-State Studies
Patients visited their centers for laboratory evaluation and physical examination at regular intervals. At entry, base-line studies included a complete blood count and measurement of urea nitrogen, creatinine, aspartate aminotransferase, alanine aminotransferase, alkaline phosphatase, and uric acid. The results analyzed in this report were obtained at entry, not during illness.
Acute Events
Patients who received acute care at hospitals not participating in the study were excluded from analysis (Table 1 ). An episode of pain was defined as the occurrence of pain in the extremities, back, abdomen, chest, or head that lasted at least two hours, led to a clinic visit, and could not be explained except by sickle cell disease. If the patient was old enough to judge whether the pain was of the type usually associated with a crisis and reported such pain, or if a young child had irritability accompanied by pain on palpation, this was considered appropriate evidence of a crisis. This working definition excluded hand—foot syndrome, chest syndrome, right upper quadrant syndrome, and osteomyelitis, as well as any episode of pain that was treated entirely at home.
Statistical Analysis
Descriptive Statistics
The "pain rate" was calculated by dividing the number of episodes by the number of patient-years. Episodes that occurred within a two-week period were counted as one episode. Seventy-four patients had more than 10 closely spaced episodes, making it difficult to determine an accurate pain rate because the boundaries between the end of one episode and the beginning of another were blurred. These patients were therefore formally excluded from the present analysis, but when we counted each of their bursts of closely spaced visits as a single episode, the overall results were unchanged (data not shown).
Pain and Mortality
The relation between the pain rate and mortality was examined with the use of a modified product-limit approach to compare the survival of patients with different pain rates.6 The resulting survival curves are analogous to life tables for patients who were alive at the age of 20. Events during the last year of follow-up were excluded from the calculation of the pain rate to avoid biasing the comparisons with premorbid changes in the pain rate. Accidents and homicides were treated as censored observations. Because of the shape of the pain rate—age curve (discussed below), data on patients who entered the study at 10 to 19 years of age were analyzed separately from the data on those who entered when 20 or older. Log-rank statistics were calculated with the 2L program of BMDP.7
Modeling the Pain Rate
To identify and quantitate factors that influenced the pain rate, wc used Poisson regression (with GLIM [Generalised Linear Interactive Modelling]), with correction for overdispersion.8 9 10 11 We included patients with sickle cell anemia whose alpha-gene status was known and excluded those under five years of age to avoid age-related changes in the complete blood count and fetal hemoglobin level. Patients for whom any covariate was missing were excluded (Table 1); data on them were compared with data on the patients included for modeling, and a t-test showed that their average pain rates were not significantly different (data not shown). Patients with a hemoglobin level above 7 mmol per liter ( 11 g per deciliter) were considered to be potentially misclassified and were therefore excluded. The confounding variables were age, sex, and clinical center. The variables considered the most important candidates for predictors were tested first (hemoglobin level, hematocrit, mean cell volume, number of red cells, percentage of fetal hemoglobin, and presence or absence of α-thalassemia). Once the significance (likelihood ratio) of these variables was determined, the rest were tested in models that included the significant terms. Variables were then sequentially removed, and terms with a significance level of 0.05 were retained to produce a final model.
All P values presented are two-tailed. Type I error rates were controlled with use of Bonferroni corrections.12
Results
Pain Rate and Genotype
Figure 1Figure 1
Distribution of Pain Rates among Patients with Sickle Syndromes. shows the pain rates in the four hemoglobinopathy groups and the distribution of episodes among the patients within each group. We further examined the patients with sickle cell anemia who averaged 3 to 10 episodes a year and found that although they represented only 5.2 percent of the group, they accounted for 32.9 percent of episodes.Sickle Cell Anemia
Pain Rate and Age
Figure 2Figure 2
Age-Specific Pain Rates (Episodes per Patient-Year) among Male (Dashed Line) and Female (Solid Line) Patients with Sickle Cell Anemia. and Table 2Table 2
Distribution of Pain Rates among Patients with Sickle Cell Anemia, According to Age. show the relation between the pain rate and age in the group with sickle cell anemia. Figure 2 implies that the pain rate increased as patients grew older, from 0 to 30 years, and declined thereafter. The rates for patients 20 to 29 years old were significantly higher than those for patients 0 to 9, 40 to 49, or ≥50 years old (data for Poisson regression not shown). However, this cross-sectional analysis may be misleading. To determine whether, on average, individual patients actually had worsening or improvement with time, we evaluated average individual trends in the pain rate among patients with at least six years of follow-up. Table 3Table 3
Trends in the Average Pain Rate in Individual Patients with Sickle Cell Anemia. summarizes the data obtained when the pain rate in individual patients dur'ing the first three years of observation was compared with the rate during the next three or more years. Among patients less than 20 years of age, the pain rate was consistently higher during the second period than during the first period, whereas among those over 20, the rates during these periods were not significantly different (even when 5-year age categories were combined to increase the sample).Pain and Mortality
No relation between mortality and the pain rate was detected among patients who entered the study when 10 to 19 years of age (Table 4Table 4
Pain Rate and Mortality among Patients with Sickle Cell Anemia.), although the small number of deaths in this age group limited the statistical power of the analysis. Mortality did vary with the pain rate among patients more than 20 years old; it was elevated among those with the highest pain rate (Fig. 3Figure 3
Survival of Patients with Sickle Cell Anemia (≥=20 Years Old at Entry) Who Had Different Pain Rates.).Risk Factors for Pain
When we controlled for age, sex, and clinic, we found that of all the laboratory variables tested, only the hematocrit and the fetal hemoglobin level emerged as important risk factors for pain (Table 5Table 5
Summary of Poisson Model for Pain Rate in Sickle Cell Anemia.). The pain rate varied directly with the hematocrit and could be modeled with the equationrate = exp[A + 0.086 (hematocrit)],
where A depends on the patient's age, fetal hemoglobin level, clinic, and sex (Table 5). α-Thalassemia in itself had no influence on pain. The slight increase in the pain rate associated with α-thalassemia was attributable to the slightly higher hematocrit of patients with this hemoglobinopathy. The same direct relation between hematocrit and pain was observed whether or not α-thalassemia was present (data not shown).
The pain rate varied inversely with the square of the fetal hemoglobin level and could be modeled with the equation
rate = exp[B —0.0032 (fetal hemoglobin)2],
where B depends on the patient's age, hematocrit, clinic, and sex (Table 5).
Discussion
Pain is the most common cause of acute morbidity in sickle cell disease and signals underlying sudden marrow ischemia or necrosis.13 , 14 Our analysis of the epidemiology of pain in a contemporary, prospective study of 3578 patients (the Cooperative Study of Sickle Cell Disease) strengthens some previously held clinical impressions but also sheds new light on the variation in disease severity, the influence of hematologic factors on severity, and implications for survival.
The patients with sickle cell anemia or sickle β0-thalassemia had more episodes of pain (Fig. 1) and a higher degree of anemia (data not shown) than the patients with hemoglobin SC disease or sickle β+-thalassemia. These observations correlate with the tendency of hemoglobins S, C, and A to polymerize and suggest that the severity of both hemolysis and clinical vasoocclusion varies directly with the tendency toward polymerization. This pattern was evident when we compared patients with different genetic sickle syndromes, but did not apply when we compared patients within the group with sickle cell anemia.
Figure 1 shows how poorly the average pain rate for a diagnosis group (genotype) reflects the rates of individual patients. Each group contained many asymptomatic patients and various percentages of patients with higher pain rates. The proportion of asymptomatic patients was underestimated in this study because its subjects (except for the newborns) were recruited through hospitals and not through population-based surveys. Two important clinical points can be drawn from our data: some patients with "mild" syndromes (hemoglobin SC disease or sickle β+-thalassemia) have a higher pain rate than some patients with the more severe syndromes (sickle cell anemia or sickle β0-thalassemia), and many patients, particularly children, do not seek treatment for pain at all, even those with sickle cell anemia.
In an average five-year period, 38.5 percent of the patients with sickle cell anemia did not seek medical attention for treatment of pain (Fig. 1). A similar proportion of asymptomatic patients was observed by Baum and coworkers in Jamaica15 and by Vichinsky and coworkers in California.16 These findings may be greeted with considerable skepticism by hospital-based physicians, whose experience has suggested that most patients tend to have multiple episodes. The 38.5 percent of asymptomatic patients were "invisible," and the 5.2 percent of patients who averaged 3 to 10 episodes of pain a year accounted for 32.9 percent of the episodes treated by physicians at hospitals.
The cross-sectional data in Figure 2 suggest that the pain rate increased until patients reached their third decade, and then declined. However, we discovered that although on average, individual patients' rates did increase with time among those under the age of 20, there was no significant trend among those 20 or older (Table 3). As discussed below, a possible explanation of the observed lower pain rate among older patients is that patients over 20 with high pain rates tend to die prematurely.
The survival curves for patients with sickle cell anemia who were 20 years of age or older, stratified according to pain rate (Fig. 3 and Table 4), demonstrated a significant relation between the pain rate and death. Patients with an average of three or more episodes per year had a higher mortality rate than those with fewer than three episodes per year. A high pain rate is a marker for early death in these young adults. We saw no correlation between pain and mortality in patients less than 20 years old, confirming the analysis of Leikin and his coworkers.17 However, the relatively small number of deaths in this age group may have prevented us from finding a significant correlation.
The data of Powars and Chan suggest that patients with high pain rates tend to continue to have high rates even over long periods of follow-up.18 Because we observed our patients for an average of only 5.13 years, we cannot answer the very important question, Will children with high pain rates have high rates as adults, and therefore be at high risk? This question is being addressed by follow-up of the original cohort of newborns in this study.
The large Jamaican study15 and a smaller study by Lande and colleagues in California19 pointed out an apparent paradox: patients with sickle cell anemia whose anemia is more severe have fewer episodes of pain. Our Poisson model (after controlling for age, sex, and fetal hemoglobin level) confirmed that the pain rate varied directly with hematocrit — an example of divergence between clinical severity and hematologic severity. The lower blood viscosity of the patients with more severe anemia may ameliorate the severity of vasoocclusion. The correlation between the hematocrit and the pain rate may have obscured the pathophysiologic importance of certain characteristics of red cells, since any property associated with a higher hematocrit may correlate with increased severity. For example, the following, logically beneficial conditions are ironically associated with high pain rates: a low percentage of dense cells, 19 , 20 a high degree of cell deformability,19 , 21 and a low percentage of irreversibly sickled cells.19
In our study population as well as other populations, the presence of α-thalassemia lowered the rate of hemolysis in patients with sickle cell anemia.22 The slight increase in the pain rate among these patients is attributable to their higher hematocrits. When we controlled for the hematocrit, α-thalassemia did not contribute to the model for the pain rate; and when we grouped the patients according to whether they had thalassemia or not, the hematocrit was found to be a predictor of pain in each group.
Fetal hemoglobin has an efficient inhibitory effect on both the extent23 and kinetics24 of hemoglobin S polymerization. Powars and coworkers studied the effect of fetal hemoglobin on pain and determined that no ameliorative effect occurred until the fetal hemoglobin level exceeded 20 percent.25 This was an unexpected finding, considering that no threshold effect on polymerization inhibition has been observed in vitro. We found (after controlling for age, sex, and hematocrit) that the fetal hemoglobin level had a strong influence on the pain rate, without a threshold effect. Increments in the fetal hemoglobin level were beneficial even when the level was low. For example, the estimates in Table 5 predict that a population of 24-year-old women with sickle cell anemia who have a hematocrit of 0.25 and a fetal hemoglobin level of 0.15 would have an average pain rate (0.7 episode per year) half that of a similar group with a fetal hemoglobin level of 0.05 (1.4 episodes per year). This difference in the average pain rate is comparable to the difference in the average pain rate between patients with sickle cell anemia and patients with hemoglobin SC disease (Fig. 1). This observation has implications for therapy with drugs, such as hydroxyurea, that increase the production of fetal hemoglobin. The model predicts that even moderate increases in the fetal hemoglobin level can reduce the pain rate, as suggested by the clinical experience of Charache and colleagues,26 and may ultimately improve survival.
Supported by the Cooperative Study of Sickle Cell Disease, a program of the Sickle Cell Disease Branch of the National Heart, Lung and Blood Institute. The following are members of the Cooperative Study of Sickle Cell Disease: participating investigators: R. Johnson, Alta Bates Hospital (Oakland, Calif.); L. McMahon, Boston City Hospital (Boston); O. Platt, Children's Hospital (Boston); F. Gill and K. Ohene Frempong, Children's Hospital (Philadelphia); G. Bray, J.F. Kelleher, and S. Leikin, Children's Hospital National Medical Center (Washington, D.C.); E. Vichinsky and B. Lubin, Oakland Children's Hospital (Oakland, Calif.); A. Bank and S. Piomelli, Columbia–Presbyterian Hospital (New York); W. Rosse, J. Falletta, and T. Kinney, Duke University (Durham, N.C); L. Lessin, George Washington University (Washington, D.C.); J. Smith and Y. Khakoo, Harlem Hospital (New York); R.B. Scott, O. Castro, and C. Reindorf, Howard University (Washington, D.C.); H. Dosik, S. Diamond, and R. Bellevue, Interfaith Medical Center (Brooklyn, N.Y.); W. Wang and J. Wilimas, LeBonheur Children's Hospital (Memphis, Tenn.); P. Milner, Medical College of Georgia (Augusta); A. Brown, S. Miller, R. Rieder, and P. Gillette, State University of New York Downstate Medical Center (Brooklyn); W. Lande, S. Embury, and W. Mentzer, San Francisco General Hospital (San Francisco); D. Wethers and R. Grover, St. Luke's–Roosevelt Medical Center (New York); M. Koshy and N. Talishy, University of Illinois (Chicago); C. Pegelow and P. Klug, University of Miami (Miami); M. Steinberg, University of Mississippi (Jackson); A. Kraus, University of Tennessee (Memphis); H. Zarkowsky, Washington University (St. Louis); C. Dampier, Wyler Children's Hospital (Chicago); and H. Pearson and A.K. Ritchey, Yale University (New Haven, Conn.); statistical coordinating centers: P. Levy, D. Gallagher, A. Koranda, Z. Flournoy-Gill, and E. Jones, University of Illinois School of Public Health (Chicago), 1978–1989; S. McKinlay, O. Platt, D. Gallagher, and D. Brambilla, New England Research Institute (Watertown, Mass.), 1989–1990; and M. Espeland, Bowman—Gray School of Medicine (Winston-Salem, N.C); program administration: M. Gaston, C Reid, and J. Verter, National Heart, Lung and Blood Institute (Bethesda, Md.).
We are indebted to Jesse Berlin, Samuel Charache, Mark Espeland, Dianne Gallagher, Sonja McKinlay, Joel Verter, and Harold Zarkowsky for their constructive criticism.
Source Information
From Children's Hospital, Dana–Farber Cancer Institute, and Harvard Medical School, Boston (O.S.P.); New England Research Institute, Watertown, Mass. (B.D.T., D.J.B.); Medical College of Georgia, Augusta (P.F.M.); Duke University School of Medicine, Durham, N.C. (W.F.R., T.R.K.); and Oakland Children's Hospital, Oakland, Calif. (E.V.). Address reprint requests to Dr. Platt at Children's Hospital, Division of Hematology/Oncology, 300 Longwood Ave., Boston, MA 02115.
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