Blood Transfusions as a Risk Factor for Non-Hodgkin's Lymphoma in the San Francisco Bay Area: A Population-based Study
Eric J. Chow1 and
Elizabeth A. Holly2,3
1 School of Medicine, University of California, San Francisco, CA.
2 Department of Epidemiology and Biostatistics, School of Medicine, University of California, San Francisco, CA.
3 Department of Health Research and Policy, Stanford University School of Medicine, Stanford, CA.
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ABSTRACT
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The incidence of non-Hodgkin's lymphoma (NHL) has risen dramatically over the past 50 years. In the search for new risk factors, blood transfusions have been investigated and shown to be associated with subsequent lymphoma in some studies. The authors tested this association in a population-based, case-control study conducted between 1988 and 1995 in the San Francisco Bay Area of California. A total of 1,591 histologically confirmed adult cases of NHL were included in this study. Cases were frequency matched to 2,515 control participants by sex, county of residence, and 5-year age intervals. Multivariate logistic regression models were used to examine the impact of possible confounders. Persons who reported a history of allogeneic transfusion were not at increased risk of NHL in this population (odds ratio (OR) = 1.0, 95% confidence interval (CI): 0.84, 1.2). No significant associations were seen when lymphomas were stratified by histologic subtype, grade, or latency period. However, autologous transfusions were associated with a decreased risk (OR = 0.39, 95% CI: 0.16, 0.94). In summary, these findings are similar to those of prior negative studies and do not support some previous reports of an adverse association between blood transfusion and NHL.
blood transfusion; case-control studies; lymphoma, non-Hodgkin; risk factors
Abbreviations:
CI, confidence interval; HIV, human immunodeficiency virus; NHL, non-Hodgkin's lymphoma; OR, odds ratio
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INTRODUCTION
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The incidence of non-Hodgkin's lymphoma (NHL) in the United States and Western Europe has risen by at least 100 percent over the past 50 years (1
, 2
). In contrast, the incidence rates of other immune system cancers such as Hodgkin's disease, multiple myeloma, and chronic lymphocytic leukemia have remained relatively stable over the past 30 years (1
, 2
). A total of 56,200 new cases of NHL were expected in 2001 with 26,300 deaths (3
). The prevalence of known NHL risk factors such as autoimmune conditions and immune suppression, including human immunodeficiency virus (HIV) infection, has not changed sufficiently to explain the increase in NHL (4
). Suggestive evidence links lymphoma with various occupational and environmental exposures, such as organophosphate insecticides, phenoxy herbicides, and other chemicals (5
, 6
). However, when these medical and occupational risk factors are considered collectively, more than half the increased NHL incidence remains unaccounted for, even after adjusting for diagnostic improvements and new classification systems (4
, 7
, 8
).
The prevalence of blood transfusion has increased dramatically in recent decades. Between 1970 and the mid-1980s, the number of red blood cell and whole blood units transfused increased by over 60 percent in the United States with adjustment for population growth (9
). However, since then the number of transfused units has decreased slightly, the decline being attributed to concern about HIV and other blood-borne diseases, changing clinical guidelines that have set higher thresholds for when to transfuse, and improved blood-conservation techniques (10
). Interest in transfusions and their possible relation to NHL arose after a 1993 prospective cohort study reported a twofold elevated risk of NHL after transfusion (11
). Within a year, two other cohort studies that reported risks of similar magnitude also were published (12
, 13
).
The biologic mechanisms linking transfusion to subsequent lymphoma are hypothesized to involve transfusion-borne oncogenic viruses (14
), transfusion-associated immune suppression (15
, 16
), or engraftment of allogeneic lymphoma cells from a donor with subclinical NHL (17
, 18
). These mechanisms may be complementary as transfusion-induced immune suppression may result in increased susceptibility to infection or allogeneic cell engraftment.
Nine epidemiologic studies on blood transfusion and NHL have been identified, all published within the last decade. The first four published studies all found an association between transfusions and an elevated risk of lymphoma (11
13
, 19
). The five studies published subsequently found no association in four instances (20

23
) and a borderline decreased risk in one instance (24
). We conducted a large, population-based, case-control study in an attempt to clarify whether an association exists between transfusion and subsequent NHL.
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MATERIALS AND METHODS
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Study participants
Detailed methods have been published about our study conducted between 1988 and 1995 (5
, 25
27
). Briefly, most persons with NHL were identified within a month of diagnosis using the Northern California Cancer Center's rapid case ascertainment system. A total of 1,591 eligible patients spoke English, were alive, were residents in one of six San Francisco Bay Area counties, and were between 21 and 74 years of age at the time of diagnosis for a 72 percent response rate. An independent pathology review was conducted to confirm NHL diagnoses. A total of 2,515 control participants between the ages of 21 and 74 years were selected from the same geographic region using random digit dialing and completed interviews for a 78 percent response rate. Controls were frequency matched to cases by sex, county of residence, and 5-year age intervals.
Trained staff used structured questionnaires to conduct face-to-face interviews in participants' homes. No proxy interviews were conducted. Study participants reported on basic demographic information, family and personal medical history, lifestyle factors, and occupational and environmental exposures. Regarding transfusion history, subjects were asked, "Not including the last year, have you ever had any blood transfusions, or received any blood products, such as factor VIII, which is a clotting agent?" If subjects answered yes, they were asked to specify the type of exposure. Subjects also were asked how many times they had received blood transfusions or blood products, their age at exposure, and the type of transfusion. Exposures and activities that occurred within 1 year of diagnosis (cases) or interview (controls) were excluded. Subjects were not asked why they were given transfusions, although some volunteered that information and their answers were recorded.
Statistical analysis
We computed 95 percent confidence intervals and odds ratios as estimates of the relative risk of NHL associated with relevant factors. All analyses were adjusted for sex and age. Heterogeneity among strata was assessed using a chi-square test with a conservative limit of p < 0.20. Trend was assessed using a chi-square test for linear trend.
Potential confounders were identified and included along with first-order interaction terms in an unconditional logistic regression model that considered transfusions as the primary risk factor of NHL. Interaction terms were eliminated using a backward stepwise procedure to develop a parsimonious model, so long as the restricted model described the data no worse than did the full model at p > 0.05. Fit was determined by the likelihood ratio test.
Potential confounders were removed from the multivariate model if they did not affect the magnitude of the odds ratio. As a result, factors reported as associated with NHL in earlier analyses, such as body mass index, education, number of vaccinations, number of bee stings, history of blood disorders/anemias, autoimmune disease, and history of other cancers, were excluded from the final multivariate model (25
). There were minimal differences in the overall results by HIV status, but HIV was kept in the models because there were slight differences by histologic type. The final model included age, sex, and HIV status. All calculations were done using STATA software (Stata Corporation, College Station, Texas).
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RESULTS
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Previous analyses had shown that selected demographic characteristics of case and control populations were similar for income and race (25
, 26
). HIV-positive subjects were disproportionately represented among the cases, comprising 18 percent of cases compared with 4 percent of controls (table 1). In both groups, those with HIV were overwhelmingly homosexual men (94 percent of HIV-positive cases and 99 percent of HIV-positive controls). Only 34 HIV-positive participants received allogeneic transfusions, none received autologous transfusions, and nine could not recall their transfusion history. Cases were more likely to have reported a history of blood disorders and anemia (odds ratio (OR) = 1.3, 95 percent confidence interval (CI): 1.1, 1.6). Cases and controls were similar relative to their history of rheumatologic conditions, diabetes, and history of other cancers. Earlier reports had addressed the distribution of various occupational and environmental exposures in relation to NHL in this population (5
, 25
27
). Overall, 13 percent of cases and controls reported having received one or more allogeneic transfusions. Compared with the unexposed, those who had received transfusions tended to be older women and heterosexual men with a history of another cancer (table 2). Differences between autologous and allogeneic transfusions showed that those receiving autologous transfusions tended to have been exposed more recently and at an older age.
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TABLE 1. Selected demographic characteristics of study participants with non-Hodgkin's lymphoma and of controls, San Francisco Bay Area, California, 19881995
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TABLE 2. Selected demographic characteristics of non-Hodgkin's lymphoma cases and controls by transfusion status, San Francisco Bay Area, California, 19881995
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In the univariate analyses, those who received allogeneic transfusions did not experience an increased risk of NHL compared with the unexposed (OR = 1.0, 95 percent CI: 0.84, 1.2). Risks of NHL associated with a history of blood transfusion adjusted for age and sex alone, and then in combination with HIV status, did not differ greatly from those of the univariate analyses (table 3). Autologous transfusions were associated with a significantly reduced risk of lymphoma (OR = 0.39, 95 percent CI: 0.16, 0.94). This association remained after multivariate adjustment.
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TABLE 3. Odds ratios and 95% confidence intervals for non-Hodgkin's lymphoma associated with blood transfusion status, San Francisco Bay Area, California, 19881995
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Stratification of the data by the number of allogeneic transfusion episodes showed no dose-response effect or trend toward an effect (p for trend = 0.48) (table 4). When data were stratified by latency between allogeneic exposure and subsequent lymphoma, no statistically significant association was found at any of the a priori determined time intervals. The risk was highest 1115 years after exposure (OR = 1.5, 95 percent CI: 0.88, 2.4), with latency beyond 15 years not associated with increased risk. Those receiving transfusions 12 years before lymphoma diagnosis or interview (data not presented in table) were not at increased risk (OR = 1.3, 95 percent CI: 0.47, 3.8; multivariate adjustment: OR = 0.83, 95 percent CI: 0.26, 2.6). Too few persons received autologous transfusions (n = six cases, 24 controls) to make stratification meaningful.
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TABLE 4. Odds ratios and 95% confidence intervals for non-Hodgkin's lymphoma associated with the number of allogeneic transfusion episodes, time interval between first allogeneic transfusion and disease, and year allogeneic blood was first transfused, San Francisco Bay Area, California, 19881995
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There was a suggestion of a period effect associated with allogeneic transfusions prior to 1940 with a greater than twofold risk of lymphoma (OR = 2.4, 95 percent CI: 0.71, 7.8) that remained elevated after multivariate adjustment (table 4). However, the sample size was small and confidence intervals overlapped unity. All the odds ratios for allogeneic transfusions that occurred in the subsequent intervals were near one and remained nonsignificant in the multivariate analysis.
When cases were stratified by the Working Formulation classification (28
), a twofold increased risk was associated with diffuse small-cell lymphoma (OR = 2.0, 95 percent CI: 1.1, 3.6; table 5). However, with adjustment for relevant factors, this risk was reduced (OR = 1.5, 95 percent CI: 0.84, 2.8). In contrast, allogeneic transfusions were associated with a reduced risk of follicular small-cell tumors after multivariate adjustment (OR = 0.46, 95 percent CI: 0.25, 0.88). Although not part of the Working Formulation, no increased risk was associated with mycosis fungoides (OR = 0.79, 95 percent CI: 0.32, 1.9).
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TABLE 5. Odds ratios and 95% confidence intervals for non-Hodgkin's lymphoma associated with allogeneic blood transfusions, stratified by Working Formulation grade and subtype, San Francisco Bay Area, California, 19881995
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DISCUSSION
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Our null results support recent work (20


24
) that contradicts the findings of four earlier positive studies (11
13
, 19
). Of these four, the first three were cohort studies. In 1993, an increased risk of lymphoma after transfusion was reported in a cohort of 37,000 women from Iowa (11
). In 5 years of follow-up, there were 68 participants with NHL and a relative risk of 2.2 (95 percent CI: 1.4, 3.6). Two updates published since then have reported attenuated but still significantly elevated risks associated with transfusions (29
, 30
). After 12 years of follow-up and 229 cases, the relative risk was 1.6 (95 percent CI: 1.2, 2.1) (30
). A Swedish cohort consisting of 3,177 blood recipients exposed in 1981 and 1982 had 13 cases of malignant lymphoma (NHL, Hodgkin's disease, and multiple myeloma) after 10 years of follow-up (12
). The authors reported a standardized morbidity ratio of 2.7 (95 percent CI: 1.4, 4.6). They also examined a second cohort of 30,000 hospitalized patients exposed during the same period and reported 29 NHL cases with a relative risk of 3.5 (95 percent CI: 1.5, 7.9) (12
). Some of these cases were the same as those in the prior cohort. A British cohort of 12,000 persons who had received perinatal transfusions was followed for an average of 28 years (13
). Those persons who had received transfusions had twice the expected standardized morbidity rate of NHL compared with the national rate. However, this result was based on five cases and was not statistically significant. The authors did not mention the effect of transfusions given later in life. NHL was the only cancer with a standardized morbidity ratio greater than two among subjects receiving transfusions.
All the other reports that examined the association between transfusion and NHL used case-control designs. A population-based study with 280 Swedish cases conducted between 1991 and 1995 reported an age- and sex-adjusted odds ratio of 1.7 (95 percent CI: 1.2, 2.4) associated with any transfusion (19
). In contrast, the five most recent case-control studies found no increased risk of NHL associated with transfusions. No association was found between transfusion and NHL (n = 260) or chronic lymphocytic leukemia (n = 101) in a Swedish case-control study that was nested within a national hospital-based cohort (20
). Their results were not modified by the amount transfused nor by adjusting for the latency period between cohort entry and lymphoma diagnosis. Lymphoma incidence was the focus in a cohort of pregnant Swedish women with bleeding complications (21
). The cohort as a whole showed no elevated standardized morbidity ratio for NHL, but odds ratios were not computed for their nested case-control study because none of the 15 lymphoma cases had received transfusions. In a Los Angeles County study that focused on acquired immunodeficiency syndrome-associated lymphoma, no significantly elevated risks were found for either HIV-negative (n = 378) or HIV-positive (n = 50) NHL cases (22
). Their estimates did not change after adjusting for the number of transfusion episodes. In Minnesota, investigators did extensive medical chart reviews and found that transfusion was not a risk factor for their 221 NHL cases (23
). Stratification by tumor grade or number of transfusions showed no significant associations. Finally, an Italian study with 385 cases found a borderline reduced risk (OR = 0.6, 95 percent CI: 0.4, 1.0) when compared with hospital controls (24
).
These studies differed in design, population, exposure, and disease assessment and in their evaluation of confounders. However, they all examined predominantly Caucasian populations in Western developed nations. They have their strengths and limitations but none is seriously flawed, making it difficult to reconcile the different conclusions (31
, 32
). However, the earlier positive studies generally had fewer cases (n = 556) compared with the subsequent null reports (including this study, n = 2,902).
Exposure assessment
In distinguishing between allogeneic and autologous transfusions, we hypothesized that autologous blood should not carry the same infectious and immune-modulating risk as allogeneic transfusions. Although neither was associated with increased risk in our study, autologous blood surprisingly was associated with a decreased risk. Autologous transfusion may be a proxy for health, as only healthier persons tend to undergo elective surgery where such transfusions are used.
Increasing exposure was not associated with increased risk in our study or three other null studies (20
, 22
, 23
) that examined dose response by the number of transfusion episodes. In addition, two of these studies also examined dose response by the volume of transfused blood and found no significantly elevated risk (20
, 23
). None of the positive studies reported on dose-response effects. The absence of any effect argues against the existence of a threshold response.
Knowledge of when transfusions were received was important to explore possible associations between exposure latency and subsequent lymphoma. We excluded transfusions given within 1 year of diagnosis or interview because persons may have received transfusions for subclinical NHL. We expect that the 1-year exclusion period was adequate, as those exposed 12 years prior to diagnosis or interview did not have an increased risk of lymphoma. All but one of the other cited studies used at least a 6-month cutoff, and some excluded transfusions given within 3 years of diagnosis. One study did not exclude any exposures on this basis and reported a slightly greater risk in those receiving transfusions within 5 years of diagnosis compared with their overall risk estimate (11
, 30
).
In our study, persons were not at increased risk during any latency intervals, although the odds ratios were slightly elevated for the 6- to 10-year and the 11- to 15-year latency periods, with a peak among those exposed 1115 years prior to lymphoma diagnosis. One group that reported overall null results also found no significant temporal effect (20
). However, two groups that reported overall elevated risks associated with transfusion found significantly elevated risks up to 15 years after exposure (11
, 19
, 30
). Laboratory results have shown donor leukocytes to persist in the host circulation for at least a year (33
), while other donor cell types have been found in hosts decades later (34
, 35
).
Potential sources of bias
Random misclassification of exposures biases results toward the null and is a concern with any null study. However, it seemed unlikely that persons would have had difficulty remembering whether they had received autologous versus allogeneic blood. In our study, persons may have had difficulty remembering the number of transfusions that they had received, especially if they had been exposed multiple times. However, risk was not associated with any number of transfusions in this study.
We minimized survival bias by using a rapid case ascertainment system that identified most patients within a month of diagnosis. Nevertheless, 21 percent of our cases died before they could be contacted. However, for our risk estimate to equal the twofold risk seen in many of the positive studies, half of the deceased cases would have had to report a history of transfusion, as compared with the 15 percent exposure rate among surviving cases with complete exposure histories. This large a discrepancy in exposure history seems unlikely.
The impact of confounding by transfusion-acquired HIV is likely to be minimal. Of the 395 HIV-positive persons enrolled in our study, only 34 HIV-positive subjects reported receiving an allogeneic transfusion. When all the HIV-positive subjects were excluded from the analysis, the odds ratios associated with allogeneic transfusions were unchanged (data not shown). HIV was not felt to be a major confounder in some of the other cited studies (11
, 13
, 22
).
Subtype assessment
Given the heterogeneity of NHL, transfusions may be associated with certain lymphoma subtypes (36
). Although some studies have found increased risks for various histologic subtypes (19
, 30
), other studies, including ours, have found no significant associations (22
, 23
). One of the major strengths of our study was a large number of cases, allowing meaningful stratification not just by grade but also by Working Formulation subtype. After adjustment for potential confounders, the elevated risk related to transfusions was not associated with any histologic grade or subtype.
Summary
Our large, population-based, case-control study found no significant association between allogeneic blood transfusions and subsequent NHL. Contrary to some earlier reports of increased risk among lower grade tumors, we found no consistent associations when lymphoma subtypes were examined separately (19
, 30
). Future studies of this topic will need to assess exposures in more detail. Stratification by leukocyte content, allogeneic versus autologous blood, packed cells versus plasma-rich whole blood transfusions, and so on is needed to establish a more meaningful disease-exposure relation. Similarly, given the heterogeneity of NHL, subtype information will be needed to identify subtype-specific associations. At present, the association between a history of blood transfusion and NHL remains unclear. However, if there is an elevated risk, it is small and cannot explain the increased temporal trends in NHL over the past several decades.
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ACKNOWLEDGMENTS
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This study was supported in part by grants R01-CA45614 and R03-CA89745 from the National Cancer Institute, National Institutes of Health.
The authors thank Paige Bracci for her comments and help on statistical issues.
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NOTES
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Correspondence to Dr. Elizabeth A. Holly, Department of Epidemiology and Biostatistics, University of California, 3333 California Street, Suite 280, San Francisco, CA 94118-1944 (e-mail: eaholly{at}epi.ucsf.edu).
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REFERENCES
|
---|
-
Devesa SS, Fears T. Non-Hodgkin's lymphoma time trends: United States and international data. Cancer Res 1992;52(suppl):5432s40s.[Abstract]
-
Cartwright R, Brincker H, Carli PM, et al. The rise in incidence of lymphomas in Europe 19851992. Eur J Cancer 1999;35:62733.[ISI][Medline]
-
Greenlee RT, Hill-Harmon MB, Murray T, et al. Cancer statistics, 2001. CA Cancer J Clin 2001;51:1536.[Abstract/Free Full Text]
-
Hartge P, Devesa SS. Quantification of the impact of known risk factors on time trends in non-Hodgkin's lymphoma incidence. Cancer Res 1992;52(suppl):5566s9s.[Abstract]
-
Holly EA, Lele C, Bracci P. Non-Hodgkin's lymphoma in homosexual men in the San Francisco Bay Area: occupational, chemical, and environmental exposures. J Acquir Immune Defic Syndr Hum Retrovirol 1997;15:22331.[ISI][Medline]
-
Hardell L, Lindström G, van Bavel B, et al. Some aspects of the etiology of non-Hodgkin's lymphoma. Environ Health Perspect 1998;106:67981.[ISI][Medline]
-
Banks PM. Changes in diagnosis of non-Hodgkin's lymphomas over time. Cancer Res 1992;52(suppl):5453s5s.[Abstract]
-
Holford TR, Zheng T, Mayne ST, et al. Time trends of non-Hodgkin's lymphoma: are they real? What do they mean? Cancer Res 1992;52(suppl):5443s6s.[Abstract]
-
Surgenor DM, Wallace EL, Hao SHS, et al. Collection and transfusion of blood in the United States, 19821988. N Engl J Med 1990;322:164651.[Abstract]
-
Goodnough LT, Brecher ME, Kanter MH, et al. Transfusion medicine. First of two partsblood transfusion. N Engl J Med 1999;340:43847.[Free Full Text]
-
Cerhan JR, Wallace RB, Folsom AR, et al. Transfusion history and Cancer risk in older women. Ann Intern Med 1993;119:815.[Abstract/Free Full Text]
-
Blomberg J, Möller T, Olsson H, et al. Cancer morbidity in blood recipientsresults of a cohort study. Eur J Cancer 1993;29A:21015.
-
Memon A, Doll R. A search for unknown blood-borne oncogenic viruses. Int J Cancer 1994;58:3668.[ISI][Medline]
-
Lyons SF, Liebowitz DN. The roles of human viruses in the pathogenesis of lymphoma. Semin Oncol 1998;25:46175.[ISI][Medline]
-
Klein HG. Immunomodulatory aspects of transfusion. Anesthesiology 1999;91:8615.[ISI][Medline]
-
Jensen LS. Benefits of leukocyte-reduced blood transfusions in surgical patients. Curr Opin Hematol 1998;5:37680.[Medline]
-
Catlin EA, Roberts JD, Erana R, et al. Transplacental transmission of natural-killer-cell lymphoma. N Engl J Med 1999;341:8591.[Free Full Text]
-
Bodó I, Peters M, Radich JP, et al. Donor-derived acute promyelocytic leukemia in a liver-transplant recipient. N Engl J Med 1999;341:80713.[Free Full Text]
-
Brandt L, Brandt J, Olsson H, et al. Blood transfusion as a risk factor for non-Hodgkin lymphoma. Br J Cancer 1996;73:114851.[ISI][Medline]
-
Adami J, Nyrén O, Bergström R, et al. Blood transfusion and non-Hodgkin lymphoma: lack of association. Ann Intern Med 1997;127:36571.[Abstract/Free Full Text]
-
Anderson H, Brandt L, Ericson A, et al. Blood transfusion at delivery and risk of subsequent malignant lymphoma in the mother. Vox Sang 1998;75:1458.[ISI][Medline]
-
Nelson RA, Levine AM, Bernstein L. Blood transfusions and the risk of intermediate- or high-grade non-Hodgkin's lymphoma. J Natl Cancer Inst 1998;90:17423.[Free Full Text]
-
Maguire-Boston EK, Suman V, Jacobsen SJ, et al. Blood transfusion and risk of non-Hodgkin's lymphoma. Am J Epidemiol 1999;149:111318.[Abstract]
-
Tavani A, Soler M, La Vecchia C, et al. Re: Blood transfusions and the risk of intermediate- or high-grade non-Hodgkin's lymphoma. J Natl Cancer Inst 1999;91:13323.[Free Full Text]
-
Holly EA, Lele C, Bracci PM, et al. Case-control study of non-Hodgkin's lymphoma among women and heterosexual men in the San Francisco Bay Area, California. Am J Epidemiol 1999;150:37589.[Abstract]
-
Holly EA, Lele C. Non-Hodgkin's lymphoma in HIV-positive and HIV-negative homosexual men in the San Francisco Bay Area: allergies, prior medication use, and sexual practices. J Acquir Immune Defic Syndr Hum Retrovirol 1997;15:21122.[ISI][Medline]
-
Holly EA, Lele C, Bracci PM. Hair-color products and risk for non-Hodgkin's lymphoma: a population-based study in the San Francisco Bay Area. Am J Public Health 1998;88:176773.[Abstract]
-
The Non-Hodgkin's Lymphoma Pathologic Classification Project. National Cancer Institute sponsored study of classifications of non-Hodgkin's lymphomas: summary and description of a Working Formulation for clinical usage. Cancer 1982;49:211235.[ISI][Medline]
-
Cerhan JR, Wallace RB, Folsom AR, et al. Medical history risk factors for non-Hodgkin's lymphoma in older women. J Natl Cancer Inst 1997;89:31418.[Abstract]
-
Cerhan JR, Wallace RB, Dick F, et al. Blood transfusions and risk of non-Hodgkin's lymphoma subtypes and chronic lymphocytic leukemia. Cancer Epidemiol Biomarkers Prev 2001;10:3618.[Abstract/Free Full Text]
-
Alexander FE. Blood transfusion and risk of non-Hodgkin lymphoma. (Commentary). Lancet 1997;350:141415.[ISI][Medline]
-
Vamvakas EC. Allogeneic blood transfusion as a risk factor for the subsequent development of non-Hodgkin's lymphoma. Transfus Med Rev 2000;14:25868.[ISI][Medline]
-
Lee TH, Paglieroni T, Ohto H, et al. Survival of donor leukocyte subpopulations in immunocompetent transfusion recipients: frequent long-term microchimerism in severe trauma patients. Blood 1999;93:312739.[Abstract/Free Full Text]
-
Starzl TE, Demetris AJ, Trucco M, et al. Chimerism and donor-specific nonreactivity 27 to 29 years after kidney allotransplantation. Transplantation 1993;55:12727.[ISI][Medline]
-
Bianchi DW, Zickwolf GK, Weil GJ, et al. Male fetal progenitor cells persist in maternal blood for as long as 27 years postpartum. Proc Natl Acad Sci U S A 1996;93:7058.[Abstract/Free Full Text]
-
Groves FD, Linet MS, Travis LB, et al. Cancer surveillance series: non-Hodgkin's lymphoma incidence by histologic subtype in the United States from 1978 through 1995. J Natl Cancer Inst 2000;92:124051.[Abstract/Free Full Text]
Received for publication May 15, 2001.
Accepted for publication October 25, 2001.