© The Author 2007. Published by Oxford University Press.
ARTICLE |
Second Cancer Incidence and Cause-Specific Mortality Among 3104 Patients With Hairy Cell Leukemia: A Population-Based Study
Affiliations of authors: Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Department of Health and Human Services, Bethesda, MD (MH, BEC, LBT); Laboratory of Pathology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Department of Health and Human Services, Bethesda, MD (ESJ)
Correspondence to: Michie Hisada, MD, MPH, ScD, National Cancer Institute, 6120 Executive Blvd., EPS 8008, Bethesda, MD 20892-7201 (e-mail: hisadam{at}mail.nih.gov).
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ABSTRACT |
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 TopNotes Abstract Context and CaveatsPatients and MethodsResultsDiscussionReferences |
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BACKGROUND: The introduction of new treatments for hairy cell leukemia has resulted in improved patient survival but also engendered increasing concern about the possibility of excess second cancers. The available evidence is conflicting, with most risk estimates based on sparse numbers. To our knowledge, no study has evaluated cause-specific mortality in patients with hairy cell leukemia.
METHODS: We quantified second cancer incidence and cause-specific mortality among 3104 two-month survivors of hairy cell leukemia who were reported to 16 population-based registries in the Surveillance, Epidemiology and End Results (SEER) Program between 1973 and 2002. Standardized incidence ratios (SIRs) and standardized mortality ratios (SMRs) were used to quantify the risk of second cancers and causes of death, respectively. The cumulative probability of a second cancer among survivors of hairy cell leukemia was calculated using a competing risk model. All statistical tests were two-sided.
RESULTS: Mean follow-up of hairy cell leukemia survivors was 6.5 years (range, 2 months–29.3 years). Second cancer risk was statistically significantly elevated (SIR = 1.24, 95% confidence interval [CI] = 1.11 to 1.37) compared with the general population. Survivors had statistically significantly higher risks of Hodgkin lymphoma (SIR = 6.61, 95% CI = 2.13 to 15.42), non-Hodgkin lymphoma (SIR = 5.03, 95% CI = 3.77 to 6.58), and thyroid cancer (SIR = 3.56, 95% CI = 1.30 to 7.74) and a lower risk of lung cancer (SIR = 0.63, 95% CI = 0.42 to 0.90). The cumulative probability of all second cancers was estimated to be 31.9% (95% CI = 26.2 to 37.6) 25 years after hairy cell leukemia diagnosis. Among 10 000 hairy cell leukemia patients, a total excess of about 34 cancers, including 21 non-Hodgkin lymphomas, 2 Hodgkin lymphomas, and 7 solid tumors (including 2 thyroid cancers), might be observed per year. Deaths due to solid tumors were not elevated compared with the general population (SMR = 0.9), and there were statistically significant deficits in mortality due to both cardiovascular (SMR = 0.67, 95% CI = 0.56 to 0.80) and cerebrovascular (SMR = 0.61, 95% CI = 0.38 to 0.93) disease.
CONCLUSIONS: Patients with hairy cell leukemia are at increased risk of Hodgkin lymphoma, non-Hodgkin lymphoma, and thyroid cancer. The decrease in lung cancer incidence and smoking-associated vascular mortality may reflect an inverse association of tobacco use with hairy cell leukemia. Future studies should address the roles of immunologic impairment inherent to hairy cell leukemia, treatment modalities, and other factors as codeterminants of morbidity and mortality in hairy cell leukemia survivors.
Prior knowledge New treatments had improved the prognosis of hairy cell leukemia patients, but the risk of second cancers in survivors was unknown. Design The risk of second cancers was determined by examining patient data in registries which comprise the Surveillance, Epidemiology, and End Results Program. Contribution The main finding of the study, an increased relative risk of Hodgkin lymphoma, non-Hodgkin lymphoma, and thyroid cancer in hairy cell leukemia patients, may be useful to the clinical community in the follow-up of these patients. Implications Despite elevated relative risks, the absolute risk of second cancers is small. Among 10 000 hairy cell leukemia patients, a total excess of 34 second primary cancers might be observed per year. Limitations The available data did not permit evaluation of the effect of individual treatments on second cancer risk.
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Hairy cell leukemia is a malignancy of mature B lymphocytes and accounts for about 2% of all leukemias (1). The introduction of purine analogs (2) and interferon alfa (3) as therapeutics for this disease since the 1990s has resulted in substantially improved survival. However, treatment with these agents has also been associated with increased risks of second cancers in some (2–7), but not all (8–11), studies. The relative risks of second cancers reported in various series of hairy cell leukemia patients (2–11) ranged from 0.95 to 4.33. The studies (2–10) were typically based on sparse numbers, with the exception of one study in which more than 1000 hairy cell leukemia patients were followed (the standardized incidence ratio [SIR] of second cancers in this study was equal to 1.01, 95% CI = 0.74 to 1.33) (11). Elevated second cancer risks in patients with hairy cell leukemia have been primarily attributed to decreased T-cell function caused by chemotherapy and to immune perturbations associated with the underlying disease (12). To our knowledge, no large population-based study has quantified the site-specific risks of second cancers and cause-specific mortality among patients with hairy cell leukemia, according to age, calendar year, initial treatment, and duration of follow-up.
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Patients and Methods |
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TopNotesAbstractContext and CaveatsPatients and MethodsResultsDiscussionReferences |
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Data Source and Study Sample
We evaluated the risk of second cancers among hairy cell leukemia patients who survived for at least 2 months after diagnosis and were reported to 16 population-based registries in National Cancer Institute's Surveillance, Epidemiology and End Results (SEER) Program from 1973 through 2002. The SEER Program collects and publishes cancer incidence and survival data from population-based cancer registries covering approximately 26% of the US population. To exclude synchronous cancers, person-years of observation were accrued starting from 2 months after the time of hairy cell leukemia diagnosis, consistent with standard approaches (13–15). Follow-up continued until death, diagnosis of a second cancer, or the end of the study on December 31, 2002, whichever occurred first. Sites of second cancers were classified according to the World Health Organization's International Classification of Diseases for Oncology, 2nd Edition (16).
Statistical Analysis
Expected numbers of second cancers were estimated by multiplying sex-, race-, age-, and calendar year–specific SEER cancer incidence rates (available at http://seer.cancer.gov) by the accumulated person-years at risk. Age and calendar year were divided into 5-year intervals. Overall and site-specific relative risks of second cancers were expressed as the standardized incidence ratio with 95% confidence intervals (CI), assuming a Poisson distribution for the occurrence of second cancer (17). The absolute excess risk of second cancers per 10 000 person-years was calculated as the difference between the observed and expected numbers divided by the person-years of follow-up and multiplied by 10 000. Second cancer risk was evaluated according to sex, age at hairy cell leukemia diagnosis (<40, 40–59, or 
60 years), race (white and non-Hispanic, white and Hispanic, black, or other/unknown), follow-up interval (2–11 months, 1–4 years, 5–9 years, or 10 years or longer), initial course of therapy (treatment that included any chemotherapy or other treatments), and calendar year of hairy cell leukemia diagnosis (1973–1989 or 1990–2002). The former calendar year period (1973–1989) represents an era before widespread treatment of hairy cell leukemia with nucleoside analogs. Information on therapy subsequent to the initial course of therapy and the names and doses of specific cytotoxic drugs used in initial therapy are not collected by the SEER Program.
Cumulative probabilities of second cancers were calculated using a nonparametric competing risk model (18). The cumulative probability at time t is estimated as a function of the cumulative hazards of second cancer incidence:
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where 
1(u) and 2(u) are the Nelson–Aalen estimators (19,20) for the cumulative hazard functions for second cancer incidence and the competing mortality, respectively. The corresponding standard errors were estimated using the counting process theory (20,21).
We also estimated relative risk of death as the standardized mortality ratio (SMR) with 95% confidence intervals, using US mortality rates (http://seer.cancer.gov) according to age and calendar year (both divided into 5-year intervals), sex, and race as the standard (17). All statistical tests were two-sided.
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Results |
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A total of 3104 hairy cell leukemia patients were evaluated for second cancer incidence. This group, which included 1607 five-year survivors and 749 10-year survivors, accumulated 20 050 person-years of follow-up (Table 1). The average duration of follow-up was 6.5 years (range, 2 months–29.3 years). The mean age at diagnosis of hairy cell leukemia was 57.4 years. Second cancers were diagnosed in 358 patients (SIR = 1.24, 95% CI = 1.11 to 1.37). The cumulative risk of all second cancers at 10, 20, and 25 years following diagnosis of hairy cell leukemia was 13.2% (95% CI = 11.6% to 14.7%), 24.5% (95% CI = 21.1% to 28.0%), and 31.9% (95% CI = 26.2% to 37.6%), respectively (Fig. 1).
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The risk of second cancers in hairy cell leukemia patients appeared larger in women than men (SIR = 1.57 [95% CI = 1.24 to 1.96] versus 1.17 [95% CI = 1.04 to 1.32], P = .05), due mainly to a greater number of lymphoproliferative malignancies in the former. When competing causes of deaths were taken into account, however, the cumulative probability of second cancers for men and women was comparable, i.e., 32.8% (95% CI = 26.1% to 39.6%) and 27.1% (95% CI = 18.5% to 35.7%), respectively, at 25 years of follow-up (P = .31).
Standardized incidence ratios of second cancers in the 2–11 month, 1–4 year, 5–9 year, and 10 or more year intervals after hairy cell leukemia diagnosis were 1.57, 1.35, 1.08, and 1.10, respectively (P for trend = .05). The difference in risk for patients diagnosed with hairy cell leukemia between 1973–1989 (SIR = 1.17, 95% CI = 1.01 to 1.36) and 1990–2002 (SIR = 1.30, 95% CI = 1.12 to 1.51) was not statistically significant. Risks were elevated among both the 1509 hairy cell leukemia patients who initially received chemotherapy (SIR = 1.35, 95% CI = 1.13 to 1.60) and the 1595 who did not (SIR = 1.18, 95% CI = 1.03 to 1.35).
Among the hairy cell leukemia patients who were given chemotherapy as the initial course of treatment, there was a statistically significant excess of second cancers among 1349 diagnosed during the 1990–2002 period (SIR = 1.42, 95% CI = 1.17 to 1.72). Although the risk of second cancers was not increased in the 160 chemotherapy recipients whose hairy cell leukemia diagnosis was in earlier (1973–1989) calendar years (SIR = 1.09, 95% CI = 0.70 to 1.63), the difference between the two calendar year intervals was not statistically significant (P = .26), and the number of patients in the latter group was sparse. Among 1595 hairy cell leukemia patients whose initial treatment did not include chemotherapy, the risks of second cancers were virtually identical in the two calendar year periods (SIR = 1.19 and 1.17 for 1973–1989 and 1990–2002, respectively).
Overall, hairy cell leukemia patients were found to be at increased risk for Hodgkin lymphoma (SIR = 6.61, 95% CI = 2.13 to 15.42), non-Hodgkin lymphoma (SIR = 5.03, 95% CI = 3.77 to 6.58), and thyroid cancer (SIR = 3.56, 95% CI = 1.30 to 7.74) (Table 2). Increased risks of Hodgkin lymphoma and non-Hodgkin lymphoma were also observed among 10-year survivors of hairy cell leukemia, while increased risks of thyroid cancer were confined to the first 5 years following hairy cell leukemia diagnosis. Elevated risks of Hodgkin lymphoma were found even among hairy cell leukemia patients who did not receive chemotherapy initially, although this observation was based on small numbers (SIR = 8.35, 95% CI = 2.25 to 21.38, four cases of Hodgkin lymphoma). Of 53 non-Hodgkin lymphomas diagnosed in hairy cell leukemia patients, 35 (66.0%) were of the B-cell phenotype, 5 (9.4%) were of the T-cell phenotype, and 13 were of unspecified phenotype. A statistically significant decrease in incidence of lung cancer in hairy cell leukemia patients was observed (SIR = 0.63, 95% CI = 0.42 to 0.90) (Table 2).
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Thirty hairy cell leukemia patients developed a third cancer during follow-up, of whom four had a fourth cancer. Cancer types among patients who developed a third cancer included prostate (six cases); lung (four cases); colon, cecum, and oral cavity (three cases each); non-Hodgkin lymphoma, bladder, and salivary gland (two each); testis, kidney, liver, retroperitoneum, melanoma, brain, small intestine, multiple myeloma, and nasal cavity (one each).
Hairy cell leukemia patients were at increased risk of mortality due to all cancers taken together (excluding basal cell carcinoma of the skin) (SMR = 4.09, 95% CI = 3.76 to 4.44) (Table 2), largely due to mortality from leukemia (SMR = 75.51, 95% CI = 68.21 to 83.38) and lymphoma (SMR = 10.55, 95% CI = 8.07 to 13.56), but not solid tumors (SMR = 0.90, 95% CI = 0.74 to 1.08). Excess deaths due to infectious diseases (SMR = 1.89, 95% CI = 1.10 to 3.03) and pneumonia/influenza (SMR = 1.41, 95% CI = 0.92 to 2.07) were apparent for up to 10 years after hairy cell leukemia diagnosis, with the largest risks during the first year. Overall, a statistically significant 17% deficit in mortality due to non-neoplastic diseases was found, along with reductions of more than 30% in mortality due to cardiovascular (SMR = 0.67, 95% CI = 0.56 to 0.80), cerebrovascular (SMR = 0.61, 95% CI = 0.38 to 0.93), and pulmonary (SMR = 0.66, 95% CI = 0.40 to 1.02) diseases.
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Discussion |
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Due to the inherent perturbation of the immune system associated with hairy cell leukemia, the additional immune suppression associated with newly developed chemotherapeutic agents used to treat the disease (3,4), and improved survival due to successful treatment, patients with hairy cell leukemia may be at high risk of adverse sequelae, including second neoplasms. Risks of second cancers among hairy cell leukemia patients have been examined previously, with varying results (2–11). In this population-based study of 3104 hairy cell leukemia survivors, the largest sample surveyed to date, we found a statistically significant 1.24-fold (95% CI = 1.11 to 1.37) increase in cancer risk in all survivors relative to incidence rates in the general population. However, no statistically significant difference in the risk of all cancers combined was found for patients diagnosed with hairy cell leukemia in 1973–1989 (SIR = 1.17, 95% CI = 1.01 to 1.36) and in 1990–2002 (SIR = 1.30, 95% CI = 1.12 to 1.51). Such a difference might signify an additional risk imposed by the introduction of nucleoside analogs, including fludarabine. Although excess risk of second cancers in the later period was confined to the 1349 patients who received chemotherapy, the number of patients who received chemotherapy in the earlier period was small (N = 160), and differences in risk were not statistically significant.
Our results indicate that the standardized incidence ratio of second cancers in hairy cell leukemia patients may be higher in women than in men. This is in contrast to results from a prior study of 1022 hairy cell leukemia patients (11) that reported a higher incidence of second cancers in males and those who were older. The gender-specific difference in standardized incidence ratios that we observed appears to be largely due to greater excesses of lymphatic and hematopoietic malignancies in female hairy cell leukemia patients compared with male patients, which may reflect in part differences in baseline rates for these malignancies. When competing causes of deaths were taken into account in the cumulative risk model, there was no statistically significant difference according to sex. This is explained by the fact that women with hairy cell leukemia have a somewhat higher overall mortality than men (relative hazard = 1.16, P = .05).
Because a diagnosis of hairy cell leukemia relies on a distinct clinicopathologic profile, including the detection of tartrate-resistant acid phosphatase activity in malignant cells (22), it seems unlikely that an initial diagnosis of non-Hodgkin lymphoma would be misclassified as hairy cell leukemia. However, recurrences of hairy cell leukemia in tissue have been misclassified as non-Hodgkin lymphoma (23). Thus, some diagnoses of non-Hodgkin lymphoma characterized as second malignancies in hairy cell leukemia patients may actually represent recurrences of hairy cell leukemia in lymph nodes or other sites with altered histologic appearance (23–25). The majority of second non-Hodgkin lymphomas diagnosed among hairy cell leukemia patients exhibited a B-cell phenotype. B-cell non-Hodgkin lymphoma is a common complication of immune deficiency; moreover, a rare occurrence of Epstein–Barr virus–associated large B-cell diffuse non-Hodgkin lymphoma has been reported in a hairy cell leukemia patient treated with cladribine (26).
Although fludarabine therapy for chronic lymphocytic leukemia has been linked to Epstein–Barr virus–positive mixed cellularity Hodgkin lymphoma (27), increased risks of Hodgkin lymphoma following a diagnosis of hairy cell leukemia like those seen in our study have not been reported previously. A biologic basis for an increased risk for Hodgkin lymphoma in hairy cell leukemia patients is unknown, and chance cannot be excluded as an explanation for our results. However, the elevated risks of non-Hodgkin lymphoma and Hodgkin lymphoma may result, in part, from immune perturbations inherent to hairy cell leukemia, in addition to the prolonged immune suppression caused by purine analog treatment (28). Unlike patients with a first primary non-Hodgkin lymphoma, none of the 36 141 Hodgkin lymphoma patients in the SEER database was subsequently diagnosed with hairy cell leukemia. However, the possibility of misclassification of a subsequent non-Hodgkin lymphoma in a hairy cell leukemia patient as Hodgkin lymphoma cannot be excluded.
Excesses of thyroid cancer in hairy cell leukemia patients were limited to the first 5 years following hairy cell leukemia, consistent with a surveillance effect. However, synchronous thyroid cancer and hairy cell leukemia have been reported (29), with statistically significant threefold excesses of hairy cell leukemia observed following a diagnosis of thyroid cancer in the SEER Program database, with five of six cases in males.
The types of second cancers that we observed in hairy cell leukemia patients were similar to those reported in smaller series (4,7,10,30,31). In a survey of 238 hairy cell leukemia patients treated with 2'-deoxycoformycin, 18 developed second cancers of types similar to what we observed, although overall risks of second cancers were not elevated (observed/expected = 0.95) (10). In a study of 207 hairy cell leukemia patients who were treated with a purine nucleoside analog cladribine, the most common second cancers included non-Hodgkin lymphoma, nonmelanoma skin cancer (not separately recorded in our study), malignant melanoma, and prostate cancer (7). Although a link between prostate cancer and hairy cell leukemia has not been established, in a series of more than 1000 men who underwent radical prostatectomy for prostate cancer, 13 or 1.2% were found to have a concurrent hematologic malignancy (nine chronic lymphocytic leukemias, three Hodgkin lymphomas, and one hairy cell leukemia) (31). Also, the prostatic acid phosphatase I is a known marker for prostate cancer, whereas macrophagic acid phosphatase I has been linked with hairy cell leukemia (32), and histologic detection of macrophage acid phosphatase I is used to diagnose hairy cell leukemia (22,33).
In our study, overall mortality (including deaths due to infectious diseases) after hairy cell leukemia was elevated relative to the general population. These results are consistent with the known susceptibility of hairy cell leukemia patients to bacterial, mycobacterial, fungal, and other infections (28) and agree with the findings in a separate series of 71 hairy cell leukemia patients in which infections were a major cause of death (31).
The statistically significant deficit in deaths due to non- neoplastic diseases in our study resulted from decreased mortality due to disorders that are frequently linked to smoking––cardiovascular, cerebrovascular, and pulmonary diseases. A greater than 30% reduction in risk of mortality in each of these categories (SMR = 0.67, 0.61, and 0.66 for cardiovascular, cerebrovascular, and pulmonary diseases, respectively) paralleled the statistically significant reduction in lung cancer incidence (SIR = 0.63). Our data, in conjunction with a strong inverse dose–response relation for tobacco use in hairy cell leukemia patients (12,34), are consistent with the hypothesis that smoking or its correlates may be negatively associated with the development of hairy cell leukemia. Although prior studies have consistently found a lower prevalence of smoking in hairy cell leukemia patients than in the general population (12,34), our study is the first to our knowledge to report a reduction in lung cancer risk. We could not examine the role of tobacco use on either cancer risk or mortality in this cohort because data on tobacco use are not collected by the SEER Program.
Limitations of our study include those inherent to registry-based investigations, such as incomplete therapy information and lack of detailed treatment data. In addition, our standardized incidence ratios estimates may represent an underestimate of risk because underreporting of second cancers may result from patient emigration from registry catchment areas.
Nonetheless, the current study represents the largest population-based series of second cancer incidence among hairy cell leukemia survivors and the first investigation, to our knowledge, of cause-specific mortality in this group. We found that hairy cell leukemia patients had statistically significant increases in risks of Hodgkin lymphoma, non-Hodgkin lymphoma, and thyroid cancer and that the increased risks of Hodgkin lymphoma and non-Hodgkin lymphoma persisted for more than 10 years. To our knowledge, this is the first report of statistically significant decreases in lung cancer incidence and in mortality due to smoking-associated diseases in hairy cell leukemia patients. Future studies should address the influence of such factors as changes in treatment regimens, immunologic impairment, natural history, diagnostic misclassification, and tobacco use on risk of second cancers in hairy cell leukemia patients. In the interim, it should be noted that the absolute excess risk of second cancers among hairy cell leukemia patients in the general population is small. Extrapolating from our results, among 10 000 hairy cell leukemia patients, a total excess of about 34 cancers––21 non-Hodgkin lymphomas, 2 Hodgkin lymphomas, and 7 solid tumors (including two thyroid cancers)––might be observed per year.
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NOTES |
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This research was supported by the Intramural Research Program of the Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH. All authors contributed to and take sole responsibility for the study concept, data analysis, data interpretation, and preparation of the manuscript.
We thank Jeremy Miller for computing support.
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Manuscript received April 17, 2006; revised November 22, 2006; accepted December 18, 2006.
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