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Risk Model for Severe Anemia Requiring Red Blood Cell Transfusion After Cytotoxic Conventional Chemotherapy Regimens

From the Centre Léon Bérard, Lyon; Institut G. Roussy, Villejuif; Centre Hospitalier, Chambéry; Centre R. Gauducheau, Nantes; Fondation Bergonié, Bordeaux; and Centre. Cl. Regaud, Toulouse, France.

Address reprint requests to J-Y Blay, MD, PhD, Centre Léon Bérard, 28, rue Laënnec-69008 Lyon, France; email blay{at}lyon.fnclcc.fr

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
PURPOSE: Cancer patients frequently experience anemia as a consequence of myelosuppressive therapy or bone marrow invasion.

PATIENTS AND METHODS: A risk model for chemotherapy-induced severe anemia requiring RBC transfusions (SARRT) within 31 days after the administration of chemotherapy was delineated in the cohort of cancer patients treated with chemotherapy in the Department of Medicine of Centre Léon Bérard in 1996 (CLB-1996). The risk model was tested on a series of 797 patients treated in 1997 (CLB-1997) and on 295 patients included in a multicenter prospective series (ELYPSE 1).

RESULTS: One hundred seven of the 1,051 patients of the CLB-1996 cohort (10%) experienced SARRT. In univariate analysis, only female sex, performance status greater than 1, hemoglobin level less than 12 g/dL before chemotherapy on day 1 (d1), and d1 lymphocyte count 700/µL significantly correlated with the risk of SARRT. Using logistic regression, d1 hemoglobin level less than 12 g/dL (odds ratio [OR] = 14.0; 95% confidence interval [CI], 7 to 30), performance status greater than 1 (OR = 2.2; 95% CI, 1.4 to 3.5), and d1 lymphocyte count 700/µL (OR = 1.7; 95% CI, 1.1 to 2.6) were identified as independent risk factors for SARRT. These three factors were given arbitrary risk coefficients of 3, 1, and 1 respectively, and a risk score for each individual patient was obtained by adding the coefficients. The calculated probability of RBC transfusions was 30% for patients with a score 4, and 11%, 4%, and 1% in patients with a score of 2 or 3, 1, and 0 respectively. This model was then tested and validated in the CLB-1997 and ELYPSE 1 series.

CONCLUSION: This risk index could be useful to identify patients at high risk for chemotherapy-induced SARRT who might be appropriate candidates for prophylactic erythropoietin treatment.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
CANCER PATIENTS frequently experience neutropenia and anemia after the administration of cytotoxic chemotherapy or radiotherapy or as a consequence of bone marrow invasion.¹ Anemia is a particularly frequent complication and results in decreased functional capacity and quality of life for cancer patients.¹ Severe anemia can be treated with RBC transfusion, but this procedure is associated with risks of transmission of infection, alloimmunization, reduced quality of life, and high financial costs.^2-4

The etiology of anemia in cancer patients is multifactorial. Contributing factors include poor nutritional status, bleeding, bone marrow infiltration with tumor, abnormal ferrokinetics associated with chronic disease, and hematologic toxicity of radiotherapy and chemotherapy.^5,6 In addition, circulating endogenous erythropoietin (Epo) levels are significantly lower in anemic cancer patients than in patients with a similar degree of anemia caused by iron deficiency.^7,8 The administration of cancer chemotherapy may further decrease the response to endogenous Epo in anemic cancer patients.^7,8 The ability of Epo to reduce the risk of anemia and the requirement for blood transfusions in cancer patients who receive chemotherapy has been demonstrated in several phase II and III studies.^9-11 However, prophylactic Epo treatment is expensive, and it is not known whether a prophylactic treatment to reduce RBC transfusion is cost-effective. Factors influencing the pharmacoeconomics of prophylactic Epo treatment include the identification of early predictors of response to Epo, optimal dose and schedule of Epo, costs associated with RBC transfusion, and the administration of Epo to patients at high risk for RBC transfusion.¹¹ Therefore, it is important to identify patients for whom the preventive use of Epo could be cost-effective.

Several studies have identified risk factors for severe anemia requiring RBC transfusion (SARRT), such as low baseline value of hemoglobin (Hb),^2,10,12,13 but no studies have investigated prognostic factors for anemia using a multivariate analysis of multiple parameters potentially linked to anemia. In this study, we report a multivariate analysis of risk factors for chemotherapy-induced SARRT in a cohort of cancer patients treated in the Department of Medicine of the Centre Léon Bérard (CLB) in 1996 (CLB-1996). A risk model for RBC transfusion was delineated and then validated in two distinct series of patients.

	PATIENTS AND METHODS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
Criteria for Patient Selection
The method used in this study was to delineate a risk index for SARRT in a retrospective series and to validate this index in two distinct series of patients. Thus, three distinct cohorts of patients are considered in this analysis.

In all three series, the selection criteria for patients were identical and as follows: patients were older than 17 years; patients with leukemia were excluded because of the possible contamination of peripheral blood by malignant cells; and patients receiving chemotherapy regimens administered daily were not included. Patients were not to be treated concomitantly with immunomodulatory cytokines (ie, interferon, interleukin-2, or others). High-dose chemotherapy regimens, ie, those requiring bone marrow or peripheral-blood stem-cell reinjection, were excluded. Every patient was included only once in the three series.

The retrospective group of 1996 comprised all patients treated with chemotherapy regimens in the CLB-1996 cohort who satisfied the selection criteria. There were 3,223 chemotherapy courses given to 1,116 patients. Every patient was analyzed only for his or her first course of chemotherapy. Patients previously treated outside the center were eligible. Histology, primary tumor site, chemotherapy regimen, sex, age, performance status (PS), and blood cell count on day 1 (d1) data were collected just before the administration of chemotherapy. Information about the use of RBC transfusions was also collected. Patients with a missing blood cell count at d1 (n = 65) were excluded. Therefore 1,051 (94%) of the 1,116 patients were analyzed. The risk model was established in this retrospective series.

The first validation group (CLB-1997) is the retrospective series of 797 patients treated in the CLB during 1997 who had not received chemotherapy in the CLB Department of Medicine in 1996. All patients were analyzed only for their first course of chemotherapy given in the CLB in 1997.

The second validation group (ELYPSE 1) is a multicenter prospective series of 321 patients treated with conventional chemotherapy in both general hospitals (n = 13) and comprehensive cancer centers (n = 5); 84 patients (26%) were treated in cancer centers and 237 (74%) in general hospitals. Every participating physician had to include all his consecutive patients during 1 month between November 1995 and September 1996. Only 295 (92%) of the 321 patients were analyzed because of missing data for PS (n = 24) or blood cell count at d1 (n = 2). This series has been recently reported.¹⁴ The characteristics of the three series of patients are listed in Table 1.

Criteria for RBC Transfusion
The end point of this study was the transfusion of RBC for severe anemia within 31 days after d1 of chemotherapy administration. Criteria for RBC transfusion in the CLB series and the ELYPSE 1 series were Hb count less than 8 g/dL or poorly tolerated anemia less than 10 g/dL, particularly in patients with underlying cardiac or pulmonary disease.

Chemotherapy Regimens
Chemotherapy regimens were separated into two subgroups according to the doses of drugs administered.^14-15 High-risk chemotherapy regimens, as defined in the present study, were regimens containing doxorubicin or epirubicin 90 mg/m², cisplatin 100 mg/m², ifosfamide 9 g/m², cyclophosphamide 1 g/m², etoposide 500 mg/m², or cytarabine 1 g/m² per course. These criteria were less stringent than in previous studies to include a higher percentage of patients in the high-risk group. The other subgroup included all other chemotherapy regimens.

Statistical Analysis
Risk factors for RBC transfusion were tested in univariate and multivariate analyses using the procedures of the SPSS 6.1.2 program (SPSS Inc, Chicago, IL, 1995). The correlation between a clinical or a biologic parameter and the incidence of chemotherapy-induced SARRT was analyzed using the Pearson ² test or Fisher's exact test. A logistic regression analyses, including the parameters studied in the univariate analysis, was performed using the logistic program of SPSS; a forward regression procedure was used with a P value < .05 for entry. Risk factors (eg, PS > 1) and end point (ie, RBC transfusion) were dichotomized. This multivariate analysis was performed in the 1,051 patients of the CLB-1996 series. For a given patient, the probability of experiencing an RBC transfusion was calculated using the following formula:

A risk model was established using the independent risk factors identified in this multivariate analysis. This risk model was then tested on the two cohorts of patients used as validation series, ie, CLB-1997 and ELYPSE 1.

	RESULTS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
Univariate Analysis
One hundred seven (10%) of the 1,051 patients of the CLB-1996 group received RBC transfusions because of severe anemia within 31 days after the administration of the course of cytotoxic chemotherapy. The median number of units of transfused RBC was 1 (range, 1 to 3 units). Twelve (11%) of the 107 patients received a transfusion for an anemia above 8 g/dL but lower than 10 g/dL, which was poorly tolerated. In univariate analysis, female sex, PS greater than 1, Hb level less than 12 g/dL, and lymphocyte count 700/µL immediately before the initiation of chemotherapy (d1) were found to be significantly (P < .05) correlated with the risk of RBC transfusion (Table 2). In contrast, age more than 60 years, d1 polymorphonuclear leukocyte count less than 1,500/µL, the type of chemotherapy regimen (high risk v others), regimens containing cisplatin, comorbidities that could influence the choice for blood transfusion, and the number of previous courses of chemotherapy were not significantly correlated with the incidence of RBC transfusion (Table 2). One hundred six patients (10%) had comorbidities that might have affected the indication for RBC transfusion; 47 patients (4%) had hypertension, 18 (2%) had heart disease, 10 (1%) had obstructive pulmonary disease, seven (0.7%) had peripheral arterial stenosis, six (0.6%) had tachycardia, five (0.5%) had congestive heart failure, four (0.4%) had asthma, two (0.2%) had pericarditis, two (0.2%) had pulmonary embolism, one (0.1%) major obesity, and four (0.4%) had other comorbidities.

Multivariate Analysis
A logistic regression was performed to identify independent risk factors for RBC transfusion using the parameters tested in the univariate analysis. Only three parameters were identified as independent risk factors for RBC transfusion. These parameters were d1 Hb level less than 12 g/dL (odds ratio [OR] = 14; 95% confidence interval [CI], 7 to 30), PS greater than 1 (OR = 2.2; 95% CI, 1.4 to 3.5), and d1 lymphocyte count 700/µL (OR = 1.7; 95% CI, 1.1 to 2.6).

Risk Model
A simple algorithm was established to calculate the expected risk of RBC transfusion for each patient. The parameters PS greater than 1, d1 lymphocyte count 700/µL, and d1 Hb count less than 12 g/dL, were given arbitrary risk coefficients of 1, 1, and 3, respectively. The risk index for a given patient was obtained by adding the coefficients of these three risk factors; the index ranged from 0 to 5. For example, a patient with a PS of 1, d1 lymphocyte count more than 700/µL, and d1 Hb count less than 12 g/dL has a risk index of 3. Patients with both a PS greater than 1 and d1 lymphocyte count less than 700/µL were pooled with patients who only had a d1 Hb count less than 12 g/dL; four risk groups of patients were thus defined (Table 3).

The calculated probability of receiving RBC transfusion within the 31 days after chemotherapy was 30% (95% CI, 16% to 47%) for patients with a risk index score 4 (ie, with all three risk factors, or with Hb level < 12 g/dL and either PS > 1 or lymphocyte count 700/µL); 11.4% (95% CI, 7% to 18%) for patients with a risk index score of 2 or 3 (Hb level < 12 g/dL or both PS > 1 and lymphocyte count 700/µL); 3.8% (95% CI, 3% to 5%) for patients with a score of 1 (PS > 1 or lymphocyte count 700/µL); and 1.2% (95% CI, 1.1% to 1.2%) for patients with a score of 0 (no risk factor). The difference in the probability of transfusion between the four groups was found to be highly significant in the CLB-1996 cohort (P < .000001).

Validation of the Model
This model was tested in the two series of patients used as validation samples. In the CLB-1997 series, 60 (8%) of 797 patients received RBC transfusion within 30 days after chemotherapy. The observed incidence of RBC transfusion within 31 days was 23%, 9%, 2.5%, 0.9% in the four risk groups. The incidence of RBC transfusion was significantly different (P < .000001) in these four different risk subgroups (Table 3).

In the ELYPSE 1 series, 14 (4.5%) of 295 patients received RBC transfusions. The observed incidence of RBC transfusion within 31 days after chemotherapy was significantly different (P = .001) among patients of the four risk subgroups (23%, 5%, 0%, 0%; Table 3). The observed incidence of RBC transfusion in the three series of studied patients was significantly different (107 [10%] of 1,051 v 60 [8%] of 797 v 14 [4.5%] of 295; ² = 10.1; P = .006). In contrast, the incidence of SARRT in the same four risk groups of the three different series was not significant (P > .05, using a ² test; Table 3).

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
Severe anemia induced by cytotoxic chemotherapy causes an impairment of the quality of life of cancer patients and generally requires RBC transfusion.¹ However, transfusion may induce several side effects, such as alloimmunization and transmission of infectious agents.^2-16 In addition, severe anemia also correlates with a poor survival and a poor response rate to chemotherapy in several tumor types.^12,17 The objective of the present study was to identify risk factors for chemotherapy-induced SARRT in a large population of patients with different cancer types treated with different chemotherapy regimens.

Severe anemia requiring RBC transfusion was chosen as the most relevant end point because these patients could benefit the most from a prophylactic treatment capable of preventing or reducing the incidence of severe anemia. Indeed, a substantial proportion of patients with Hb level greater than 8 g/dL receive RBC transfusion because of poor clinical tolerance or underlying co-morbidities. Previously reported risk factors for anemia in cancer patients include tumor site, baseline Hb level, RBC count, parameters of iron metabolism, and toxicity of chemotherapy.^2,10,12 However, we are unaware of reports devoted to the analysis of multiple risk factors for severe anemia induced by conventional cytotoxic chemotherapy.

Clinical or biologic parameters, which were previously found to be correlated with hematotoxicity after chemotherapy in the previous studies of the ELYPSE group (age, sex, PS, number of previous courses, blood cell counts),^14,15,18 as well as risk factors for anemia, previously reported in other reports,^2,10,12 were tested in the present work. Because this model was delineated in a retrospective series, it was not possible to test all previously reported parameters correlated with hematotoxicity. For instance, the 5-day lymphocyte count, a major risk factor for febrile neutropenia in previous studies performed in the ELYPSE group,^14,15,18 was not available in most patients of this retrospective series, although this parameter was found to be correlated with the incidence of SARRT in the ELYPSE 1 series (not shown). For practical considerations, we tested d1 lymphocyte count 700/µL instead of day 5 lymphocyte count, even though it was less strongly correlated with hematologic toxicity in previous studies.^14,18 Importantly, the parameters included in the present model are available for most patients and do not require expensive or unusual biologic investigations.

The risk model for chemotherapy-induced SARRT was established on a retrospective, but almost exhaustive (94%), cohort of patients treated in the Department of Medicine of the CLB in 1996. To avoid bias, patients were analyzed only for their first course of chemotherapy during this year. The frequency of RBC transfusion was substantial (n = 107, 10%) in this series of patients treated with conventional chemotherapy. Among the parameters tested, three were found to have an independent prognostic value for RBC transfusion, ie, Hb level less than 12 g/dL at d1, lymphocyte count 700/µL at d1, and PS greater than 1. It is noteworthy that neither the number of previous chemotherapy courses nor the use of cisplatin influenced the incidence of a significant SARRT in this series of patients. A low baseline Hb level was the strongest risk factor for anemia in this study. This is consistent with a previous study,¹⁹ which showed that patients with an initial Hb level of 11 g/dL that dropped by 1 g/dL had a greater than 90% risk for transfusion.

A risk model based on the three risk factors was established from the present study and enabled us to identify subgroups of patients with a significantly different risk of RBC transfusion in the tested series. In particular, 30% of patients with Hb level less than 12 g/dL and at least one of the other two risk factors were given RBC transfusion within 31 days after d1 of chemotherapy. Importantly, 95% to 100% of all transfused patients in the three series were included in the two highest risk groups, and 59% of all transfused patients were identified in the highest risk group among the three series tested. These results indicate that the present model identifies a small subgroup of patients (19% for the high-risk group of 2,143 patients among the three series) at high risk of SARRT within the 31 days after chemotherapy. This subgroup included the majority of all transfused patients. Importantly, this index does not rely on the number of previous courses of chemotherapy received by the patient; therefore, it could be applied to any patient matching the inclusion criteria at any time of his or her treatment program.

A potential limitation of this study is the heterogeneity of these series of patients in terms of disease types and chemotherapy regimens. The CLB-1996 and CLB-1997 series included patients with similar clinical characteristics. In contrast, the ELYPSE 1 series was a multicenter prospective cohort of patients treated with less intensive chemotherapy regimens and was probably more representative of a general oncology practice. Despite the differences in the patient characteristics and, in particular, the differences in the frequency of RBC transfusion, this index was capable of distinguishing patients with a high risk of RBC transfusion. The reproducibility of the results in the two groups used as validation samples and the large number of patients analyzed (n = 2,143) suggest that the risk model may be used to identify patients at high risk for chemotherapy-induced SARRT in the general population of patients treated with conventional chemotherapy.

It is important to note, however, that the series tested included patients treated mainly at one institution. Therefore, the model presented here deserves to be validated in other large prospective or retrospective series in other institutions. Of note, the mean number of units of transfused RBC was similar to or lower than that reported in comparable series in the literature,^2,20 which supports the relevance of this model to the general population of cancer patients treated with chemotherapy.

If its validity is confirmed by additional studies, this risk model may be used to identify patients in whom a strict surveillance of Hb count should be mandatory. In addition, this model could distinguish a cohort of patients for whom primary prophylactic administration of Epo could be both clinically justified and cost-effective.^20-22 This remains a major issue, particularly in view of a recent report that indicated that treatment with Epo improves the quality of life of patients with chemotherapy regardless of disease type and response to chemotherapy.²⁰ Randomized phase III studies could focus on the subgroup of high-risk patients identified in this study to evaluate clinical benefit and cost-effectiveness from the prophylactic use of Epo.

	APPENDIX

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 

	ACKNOWLEDGMENTS

We thank Professor Ian Tannock (Centre Léon Bérard, Lyon, France, and Princess Margaret Hospital, Toronto, Canada) for his helpful comments.

	REFERENCES

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
1. Henry DH, Thatcher N: Patient selection and predicting response to recombinant human erythropoietin in anemic cancer patients. Semin Hematol 33:2-5, 1996

2. Shillings JR, Sridhar FG, Wong C, et al: The frequency of red cell transfusion for anemia in patients receiving chemotherapy: A retrospective cohort study. Am J Clin Oncol 16:22-25, 1993[Medline]

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4. Tretiak R, Laupacis A, Riviere M, et al: Cost of allogeneic and autologous blood transfusion in Canada: Canadian Cost of Transfusion Study Group. Can Med Assoc J 154:1501-1508, 1996[Abstract]

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7. Miller CB, Jones RJ, Piantadosi S, et al: Decreased erythropoietin response in patients with anemia of cancer. N Engl J Med 322:1689-1692, 1990[Abstract]

8. Case DC, Bukowski M, Carey RW, et al: Recombinant human erythropoietin therapy for anemic patients on combination chemotherapy. J Natl Cancer Inst 85:801-806, 1993[Abstract/Free Full Text]

9. Cascinu S, Fedeli A, Del Ferro E, et al: Recombinant human erythropoietin treatment in cisplatin-associated anemia: A randomized double-blind trial with placebo. J Clin Oncol 12:1058-1062, 1994[Abstract/Free Full Text]

10. Del Mastro L, Venturini M, Lionetto R, et al: Randomized phase III trial evaluating the role of erythropoeitin in the prevention of chemotherapy induced anemia. J Clin Oncol 15:2715-2721, 1997[Abstract/Free Full Text]

11. Ludwig H, Fritz E, Leitgeb C, et al: Prediction of response to erythropoeitin treatment in chronic anemia of cancer. Blood 84:1056-1063, 1994[Abstract/Free Full Text]

12. Fein DA, Lee WR, Hanlon AL, et al: Pretreatment hemoglobin level influences local control and survival of T1-T2 squamous cell carcinomas of the glottic larynx. J Clin Oncol 13:2077-2083, 1995[Abstract/Free Full Text]

13. Hescketh PJ, Cooley TP, Finkel HE, et al: Treatment of advanced non-small cell lung with cisplatin, 5-fluorouracil, and mitomycin C. Cancer 62:1466-1470, 1988[Medline]

14. Blay JY, Ray-Coquard I, Mermet J, et al: ELYPSE 1: A multicentric prospective study of prognostic factors for febrile neutropenia after cytotoxic chemotherapy in general and cancer hospitals. Proc Am Soc Clin Oncol 16:56a, 1997 (abstr 196)

15. Blay JY, Chauvin F, LeCesne A, et al: Early lymphopenia after cytotoxic chemotherapy as a risk factor for febrile neutropenia. J Clin Oncol 14:636-643, 1996[Abstract/Free Full Text]

16. Denton TA, Diamond GA, Matloff JM, et al: Anemia therapy: Individual benefit and social cost. Semin Oncol 21:29-35, 1994

17. Coiffier B, Gisselbrecht C, Herbrecht R, et al: LNH-84 regimen: A multicenter study of intensive chemotherapy in 737 patients with aggressive malignant lymphoma. J Clin Oncol 7:1018-1026, 1989[Abstract]

18. JY Blay, LeCesne A, Mermet C, et al: A risk model for thrombocytopenia requiring platelet transfusion after cytotoxic chemotherapy. Blood 92:405-410, 1998[Abstract/Free Full Text]

19. Abels R, Larlholt K, Nelson R, et al: Risk of transfusion in small cell lung cancer patients receiving chemotherapy. Blood 84:664A, 1994 (abstr)

20. Demetri G, Kris M, Wade J, et al: Quality of life benefit in chemotherapy patients treated with epoietin alpha is independent of disease response or tumor type: Results from a prospective community oncology group. J Clin Oncol 16:3412-3425, 1998[Abstract]

21. American Society of Clinical Oncology: American Society of Clinical Oncology recommendations for the use of hematopoietic colony-stimulating factors: Evidence-based, clinical practice guidelines. J Clin Oncol 12:2471-2508, 1994[Abstract/Free Full Text]

22. Koeller JM: Clinical guidelines for the treatment of cancer-related anemia. Pharmacotherapy 18:156-169, 1998[Medline]

Submitted December 1, 1998; accepted April 22, 1999.

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This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Ray-Coquard, I. Articles by Blay, J. Y. Search for Related Content PubMed PubMed Citation Articles by Ray-Coquard, I. Articles by Blay, J. Y. Social Bookmarking                            What's this?