Original Article
Decreased Erythropoietin Response in Patients with the Anemia of Cancer
N Engl J Med 1990; 322:1689-1692June 14, 1990
- Abstract
- Abstract
Patients with solid tumors are often anemic even before they undergo cytotoxic therapy. Since the cause of the anemia of cancer is unknown, we examined the possible role of erythropoietin. Using a sensitive radioimmunoassay, we determined serum immunoreactive erythropoietin levels in 81 anemic patients with solid tumors.
For any given degree of anemia, the serum concentration of immunoreactive erythropoietin was lower in this group of patients than in a group of control patients with iron-deficiency anemia (P = 0.0001). Furthermore, the expected inverse linear relation between serum levels of immunoreactive erythropoietin and of hemoglobin was absent in the group with cancer. The erythropoietin response was further decreased in patients receiving chemotherapy; it was not influenced by the presence or absence of cisplatin in the treatment regimen. The inability of the patients with cancer to produce erythropoietin was not absolute; if they had hypoxemia, adequate erythropoietin production was restored.
We conclude that erythropoietin levels are inappropriately low in anemia associated with cancer, and that erythropoietin deficiency may contribute to the development of this form of anemia. Treatment of the anemia of cancer with erythropoietin may be of value. (N Engl J Med 1990; 322:1689–92.)
Media in This Article
Figure 1
Hemoglobin Concentrations in Relation to Serum Immunoreactive Erythropoietin Concentrations in 74 Nonhypoxemic Anemic Patients with Cancer (○) and 24 Patients with Iron-Deficiency Anemia (■).Table 1
Clinical Characteristics of 81 Patients with Cancer.Article Activity
- Article
THERE can be many causes of anemia in patients with cancer. However, such patients are often anemic even before they receive cytotoxic therapy and even if their bone marrow is not involved by tumor.1 The anemia of cancer is normochromic and normocytic, with an inappropriately low reticulocyte count. Although this anemia is usually mild (hemoglobin level >5.6 mmol per liter [9 g per deciliter]), hemoglobin values as low as 4.3 mmol per liter (7 g per deciliter) are not rare.1 2 3 4 5 Serum iron concentrations and iron-binding capacity are low, and morphologic examination of the bone marrow reveals erythroid precursors with a normal appearance and adequate or increased stainable iron. Furthermore, the anemia of cancer cannot be ascribed to a lack of erythroid progenitor cells or an unresponsiveness to erythropoietin. Early and late erythroid-progenitor cells (erythroid burst-forming and colony-forming units, respectively) from the bone marrow of patients with cancer maintain normal sensitivity to erythropoietin when cultured in vitro. The number, size, degree of hemoglobin production, and time of appearance of both types of erythroid colonies from the marrow of patients with cancer are also normal.2
Although the cause of the anemia of cancer is unknown, the hematologic picture of this disorder is similar to that of the anemia of chronic renal failure and other chronic diseases. In the anemia of chronic renal failure, the inverse linear relation between the concentrations of hemoglobin and those of circulating erythropoietin that is observed in other anemic states (iron deficiency, acute blood loss, and hemolysis) is not present.6 The use of recombinant erythropoietin has been highly successful in the treatment of patients with anemia and chronic renal failure; the majority of patients have an increase in hemoglobin level and a decrease in transfusion requirements.7 , 8 Therefore, inadequate erythropoietin production appears to contribute to the anemia of chronic renal failure.
Previous studies of erythropoietin levels in anemic patients with cancer have been inconclusive. Studies describing decreased erythropoietin response in the anemia of cancer were limited by small numbers of patients and the use of relatively insensitive bioassays.2 3 4 , 9 A sensitive radioimmunoassay for erythropoietin has been developed10; erythropoietin levels in some anemic states have been studied, and the values are available for comparison.6 Adequate erythropoietin levels in patients with cancer have been reported in two studies,11 , 12 one of which used a sensitive radioimmunoassay. However, in both studies mean erythropoietin levels in patients with cancer were compared with those in normal subjects. Analysis of mean erythropoietin levels alone is not adequate for judging the appropriateness of the erythropoietin response to anemia.13 The erythropoietin level must be correlated with the concurrent hemoglobin level and then compared with an appropriate erythropoietin response to that degree of anemia, as observed in the anemia associated with iron deficiency or hemolysis. In this study, we used a sensitive and specific commercially available radioimmunoassay to analyze the relation between erythropoietin levels and hemoglobin levels in patients with the anemia of cancer, comparing these patients with controls with iron-deficiency anemia.
Methods
We studied 81 adult patients with solid tumors and anemia (hemoglobin ≤7.4 mmol per liter [12 g per deciliter]) who were treated at the Johns Hopkins Hospital between December 1987 and June 1988. The experimental protocol was approved by the Joint Committee for Clinical Investigation of the Johns Hopkins Hospital. All the patients had normal renal function (serum creatinine ≤130 μmol per liter [1.5 mg per deciliter]). The characteristics of the patients are summarized in Table 1Table 1
Clinical Characteristics of 81 Patients with Cancer.. Seven of the patients had hypoxemia (partial pressure of oxygen <60 mm Hg) and were evaluated separately. All but 2 of the 74 patients without hypoxemia were ambulatory and capable of self-care (Karnofsky performance score ≥60 percent), and 54 (75 percent) of these 72 were outpatients. Only one patient had an active infection at the time of assay. The mean hemoglobin value in the inpatients was not different from that in the outpatients (6.2 vs. 6.5 mmol per liter [10.0 vs. 10.4 g per deciliter]; P = 0.2). The patients were categorized on the basis of their treatment history: group 1 contained patients who had not previously received cytotoxic therapy; group 2, patients who had previously received cytotoxic therapy but had not received such therapy for at least six weeks before being studied; and group 3, patients who were currently receiving chemotherapy. Patients in group 3 were further categorized on the basis of whether or not they had been treated with a regimen including cisplatin.The control group consisted of 24 men and women with iron-deficiency anemia who had been referred to the Johns Hopkins Hospital hematology clinic. Patients with iron deficiency were chosen as controls because the erythropoietin response of such patients to anemia is known and considered appropriate.3 , 6 The presence of iron deficiency was confirmed by the observation of either a serum ferritin level of less than 30 μg per liter in men or 10 μg per liter in women, or a serum iron level of less than 65 μmol per liter, a serum transferrin level of more than 4.10 g per liter, and a transferrin saturation value of less than 20 percent. All the controls had normal renal function.
Serum was collected and frozen, and immunoreactive erythropoietin was measured with a commercially available radioimmunoassay (Smith-Kline Bioscience Laboratories) that uses Radio-labeled recombinant human erythropoietin as the antigen and a single lot of polyvalent rabbit antiserum to recombinant erythropoietin. With this assay, the range of normal values in adults without anemia is 4 to 26 IU per liter; the interassay coefficient of variation ranges from 14.5 percent, when the mean serum level of immunoreactive erythropoietin is 9.6 IU per liter, to 8.6 percent, when the mean level is 99.3 IU per liter.10 The levels of serum immunoreactive erythropoietin measured with this assay correlate with the levels of biologically active erythropoietin measured with the polycythemic-mouse bioassay.10
Erythropoietin levels were analyzed in relation to concurrent hemoglobin levels in all patients. Analysis of covariance14 was used to compare the association between erythropoietin and hemoglobin levels while controlling for the effects of the underlying features of the group studied (the iron-deficiency anemia of the controls, the type of treatment, the type of cancer, and sex) and to compare the erythropoietin response defined by the slope of the line describing erythropoietin levels plotted against hemoglobin levels while adjusting for group effects. Pairwise differences between mean hemoglobin and serum immunoreactive erythropoietin levels were tested for statistical significance with the t-test. For the application of the t-test, assumption of equal variances was tested with the F statistic. When the variances in comparison groups were not equal, corrections in the t statistic and the number of degrees of freedom were made.15 All P values reported are two-sided. Erythropoietin and hemoglobin levels are reported as means ±SEM for the groups studied.
Results
Mean hemoglobin and serum immunoreactive erythropoietin levels are summarized in Table 2Table 2
Hemoglobin and Serum Immunoreactive Erythropoietin Levels in Nonhypoxemic Patients with Cancer and Patients with Iron-Deficiency Anemia.*. The mean serum immunoreactive erythropoietin level was significantly lower in the patients with cancer than in the controls, but the mean hemoglobin level did not differ significantly between the two groups. When the serum immunoreactive erythropoietin level was plotted as a function of the hemoglobin level (Fig. 1Figure 1Hemoglobin Concentrations in Relation to Serum Immunoreactive Erythropoietin Concentrations in 74 Nonhypoxemic Anemic Patients with Cancer (○) and 24 Patients with Iron-Deficiency Anemia (■).), there was a significant inverse linear relation between hemoglobin and erythropoietin levels in the controls (r = −0.71); in contrast, there was no significant correlation in the patients with cancer (r = −0.30). Specifically, serum immunoreactive erythropoietin levels did not increase as hemoglobin levels fell in this group. In addition, analysis of covariance demonstrated that at any given hemoglobin level, the erythropoietin level was significantly lower in the patients with cancer than in the controls (P = 0.0001). The sex or the type of neoplasm of the patients with cancer did not influence the erythropoietin response to anemia (data not shown). The low erythropoietin levels in the patients with cancer were not related to a generalized reduction in serum protein concentrations or impaired liver function, since there was no correlation between erythropoietin levels and serum levels of albumin (r = −0.17) or aspartate aminotransferase (r = 0.18). Over 90 percent of the patients with cancer had normal serum albumin levels, reflecting the generally good nutritional status of this group.When the three treatment-history subgroups within the group with cancer were analyzed separately, serum immunoreactive erythropoietin levels for any given degree of anemia were significantly lower in each subgroup than in the control group (the patients with iron-deficiency anemia) (P = 0.0001). Although there was no difference in mean hemoglobin and serum immunoreactive erythropoietin levels among these three subgroups (Table 3Table 3
Hemoglobin and Serum Immunoreactive Erythropoietin Levels in Nonhypoxemic Patients with Cancer.*), analysis of covariance revealed differences in the erythropoietin response to anemia as defined by the slope of the relation between the erythropoietin and hemoglobin levels. The erythropoietin response to anemia was significantly lower in the patients who were receiving chemotherapy than in the patients who received no treatment or the patients who had not received therapy for more than six weeks (P = 0.03). However, there was no significant difference in the erythropoietin response to anemia between the untreated patients and the patients not treated for six weeks. Among the patients receiving chemotherapy, the erythropoietin response to anemia in those treated with a regimen containing cisplatin did not differ from the response in those treated with a regimen that did not contain cisplatin (mean erythropoietin values after adjustment for hemoglobin levels, 37.1 ±4.4 vs. 33.2±2.9 IU per liter, respectively; P = 0.2).In the seven anemic patients with cancer who had hypoxemia, the mean serum immunoreactive erythropoietin level (279 IU per liter; median, 110; range, 70 to 1210) was not different from that in the controls (P = 0.24). Furthermore, the erythropoietin response for a given hemoglobin level in these seven patients was similar to that in the controls (P = 0.38). Therefore, the patients with cancer were able to mount an adequate erythropoietin response when stimulated by hypoxemia.
Discussion
This study defines the relation between erythropoietin and the anemia of cancer in a large group of patients with a variety of solid tumors. Our finding of an inadequate erythropoietin response in these patients is consistent with the findings of some previous small studies2 3 4 , 9 but not those of others.11 , 12 We believe the difference between our study and those that did not demonstrate inadequate erythropoietin production in patients with cancer-related anemia11 , 12 is a result of a difference in the method of statistical analysis rather than in the selection of patients. Our patients appeared to be representative of patients with anemia associated with cancer in that their mean hemoglobin level (6.4 mmol per liter [10.3 g per deciliter]) and their range of hemoglobin values (4.2 to 7.4 mmol per liter [6.7 to 12.0 g per deciliter]) were similar to those in other reports of patients with this syndrome.1 2 3 4 5 , 11 , 12 The studies that described a normal erythropoietin response in patients with cancer-related anemia11 , 12 based their conclusions on the finding that the mean erythropoietin levels in their patients were above the normal range. In fact, the mean erythropoietin levels in these studies were similar to that in our patients, which was also above the normal range. When the erythropoietin response in relation to the degree of anemia is compared with the normal response that occurs in patients with iron-deficiency anemia or hemolytic anemias, the inadequate response in the patients with cancer-related anemia becomes evident.
In addition to the inadequate erythropoietin response for a given degree of anemia in these patients, there was an absence of a linear relation between erythropoietin levels and hemoglobin levels. This absence of a correlation between hemoglobin and erythropoietin levels in patients with cancer is similar to what is seen in patients with the anemia of chronic renal failure6 but is different from what is seen in patients with other normochromic, normocytic anemias associated with chronic disease. In anemic patients with rheumatoid arthritis16 or human immunodeficiency virus (HIV) infection,17 the erythropoietin response to anemia is inadequate but the erythropoietin level continues to be inversely related to the hemoglobin level. This suggests that the normal feedback mechanism that stimulates an erythropoietin response to anemia is absent in patients with cancer or chronic renal failure, whereas the normal feedback loop is impaired but intact in patients with rheumatoid arthritis or HIV infection. The reason for the difference in erythropoietin response in morphologically similar anemias is unknown. However, we did not observe an absolute inability of the patients with cancer to respond to anemia with an increase in erythropoietin levels. We found that normal erythropoietin production was reestablished when anemic patients with cancer became hypoxemic. Similarly, certain conditions can stimulate erythropoietin production in other disease states associated with a decreased erythropoietin response to anemia. For example, in patients with chronic renal failure, either hypoxemia18 or hepatitis19 can induce marked elevations in erythropoietin levels in response to anemia. In patients with HIV-associated anemia, treatment with zidovudine results in restoration of the erythropoietin response to anemia.17
The blunted erythropoietin response in patients with cancer worsened with chemotherapy. Similar findings have been reported in a study in animals, in which erythropoietin production decreased after alkylating agents were infused directly into the kidney,20 and in a small study in patients, in which erythropoietin production was ultimately suppressed relative to the hemoglobin level after high-dose chemotherapy was administered, despite an initial rise in erythropoietin that was unrelated to anemia.21 In a study describing a decreased erythropoietin response to anemia in patients receiving chemotherapy including cisplatin,22 the inadequate response was thought to be due to cisplatin-associated nephrotoxicity. However, renal function appeared to be normal in our patients, although subclinical nephrotoxicity could not be excluded. Moreover, the erythropoietin response to anemia was similar in the patients receiving chemotherapy whether or not the treatment included cisplatin. This suggests that chemotherapy may have an effect on the erythropoietin response to anemia that is independent of therapy-induced nephrotoxicity.
The cause of the blunting of the erythropoietin response to anemia in patients with cancer is unknown. It did not appear to be specific to a type of tumor and was not related to liver or kidney disease or to a non-specific impairment of protein production in our patients. The erythropoietin response in patients with the anemia of cancer is similar to the response in patients with the anemia of chronic renal failure. This suggests that inadequate erythropoietin production is a factor contributing to the development of anemia in patients with cancer. Therefore, replacement with exogenous erythropoietin may be useful in the treatment of these patients; preliminary clinical trials have demonstrated that recombinant human erythropoietin can ameliorate the anemia associated with cancer and chemotherapy.23 24 25
Source Information
From the Johns Hopkins Oncology Center (C.B.M., R.J.J., S.P., M.D.A.) and the Department of Internal Medicine (J.L.S.), the Johns Hopkins Medical Institutions, Baltimore. Address reprint requests to Dr. Jones at Rm. 2–127, Johns Hopkins Oncology Center, 600 N. Wolfe St., Baltimore, MD 21205.
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