Rochelle E. Curtis, M.A., Philip A. Rowlings, M.B., B.S., H. Joachim Deeg, M.D., Donna A. Shriner, Pharm.D., Gérard Socié, M.D., Ph.D., Lois B. Travis, M.D., Mary M. Horowitz, M.D., Robert P. Witherspoon, M.D., Robert N. Hoover, M.D., Kathleen A. Sobocinski, M.S., Joseph F. Fraumeni, M.D., John D. Boice, Sc.D., H. Gary Schoch, B.A., George E. Sale, M.D., Rainer Storb, M.D., William D. Travis, M.D., Hans-Jochem Kolb, M.D., Robert Peter Gale, M.D., Ph.D., and Jakob R. Passweg, M.D.
Background The late effects of bone marrow transplantation,including cancer, need to be determined in a large populationat risk.
Methods We studied 19,229 patients who received allogeneic transplants(97.2 percent) or syngeneic transplants (2.8 percent) between1964 and 1992 at 235 centers to evaluate the risk of the developmentof a new solid cancer. Risk factors relating to the patient,the transplant, and the course after transplantation were evaluated.
Results The transplant recipients were at significantly higherrisk of new solid cancers than the general population (observedcases, 80; ratio of observed to expected cases, 2.7; P<0.001).The risk was 8.3 times as high as expected among those who survived10 or more years after transplantation. The cumulative incidencerate was 2.2 percent (95 percent confidence interval, 1.5 to3.0 percent) at 10 years and 6.7 percent (95 percent confidenceinterval, 3.7 to 9.6 percent) at 15 years. The risk was significantlyelevated (P<0.05) for malignant melanoma (ratio of observedto expected cases, 5.0) and cancers of the buccal cavity (11.1),liver (7.5), brain or other parts of the central nervous system(7.6), thyroid (6.6), bone (13.4), and connective tissue (8.0).The risk was higher for recipients who were younger at the timeof transplantation than for those who were older (P for trend,<0.001). In multivariate analyses, higher doses of total-bodyirradiation were associated with a higher risk of solid cancers.Chronic graft-versus-host disease and male sex were stronglylinked with an excess risk of squamous-cell cancers of the buccalcavity and skin.
Conclusions Patients undergoing bone marrow transplantationhave an increased risk of new solid cancers later in life. Thetrend toward an increased risk over time after transplantationand the greater risk among younger patients indicate the needfor lifelong surveillance.
Bone marrow transplantation is an increasingly effective treatmentfor leukemia and several other malignant and nonmalignant diseases.However, there is growing concern about possible late consequencesof compromised immune function and of treatment, particularlynew cancers resulting from the total-body irradiation and high-dosechemotherapy used as conditioning regimens for transplantation.Few studies have assessed the risk of cancer among long-termsurvivors of bone marrow transplantation.1,2,3,4,5,6,7 Somestudies have shown a high risk of lymphoproliferative disordersafter allogeneic bone marrow transplantation and statisticallysignificant excesses of myelodysplastic syndromes and leukemiaafter autologous transplantation for lymphoma.2,7 Earlier studiesof solid cancers that occurred after transplantation have beenbased on relatively small numbers of cases, and little informationwas available on individual cancers. Using a multi-institutiondata base that includes almost 20,000 recipients of allogeneictransplants, we conducted a study to determine the risk of newsolid cancers after bone marrow transplantation.
Methods
Patients
A total of 19,229 patients who received allogeneic or syngeneicbone marrow transplants (97.2 percent and 2.8 percent, respectively)were identified from the International Bone Marrow TransplantRegistry (IBMTR) and the Fred Hutchinson Cancer Research Centerin Seattle. Data from the IBMTR, which covers 234 transplantationcenters, included transplantations for the period from 1964to 1990, with follow-up through 1991; the Seattle data werefor the period from 1969 to 1992. The risk of new cancers in1980 among the patients from Seattle2 and several centers coveredby the IBMTR4,6,7 have been published previously. From the originalcohort of 19,430, we excluded 201 patients with Fanconi's anemiaand 376 with primary immunodeficiency diseases, because theyhave an inborn susceptibility to cancer.8,9
Most of the patients (75 percent) received transplants for leukemia,and most (79 percent) received bone marrow from an HLA-identicalsibling. The median age at the time of transplantation was 25.5years. Overall, 91 percent of the recipients were followed throughthe end date of the study. Among the 9501 patients who survivedfor at least 1 year after transplantation, the median durationof follow-up was 3.5 years (mean, 4.5; maximum, 25). Pathologyreports and selected slides were reviewed centrally for 95 percentof the patients with new solid tumors.
Treatment and Risk Factors
The characteristics of the patients are shown in Table 1. Forpatients with second cancers, information on prior therapy forthe primary disease was abstracted from the transplantationcenter's records, but such data were generally unavailable forthe other patients. Conditioning regimens for 14,000 patients(73 percent of the cohort) consisted of total-body irradiationcombined with cyclophosphamide-based regimens (65 percent) orother drugs (8 percent). Another 656 patients (most of whomhad aplastic anemia) received limited-field irradiation (totalnodal, total lymphoid, or thoracoabdominal irradiation), withouttotal-body irradiation. Patients who did not undergo irradiationtypically received cyclophosphamide (22 percent), with or withoutother drugs.
Table 1. Characteristics of 19,229 Patients Undergoing Bone Marrow Transplantation.
Prophylaxis against graft-versus-host disease included T-celldepletion of bone marrow; drug therapy with cyclosporine, methotrexate,corticosteroids, or other drugs; and combined therapies. Acutegraft-versus-host disease was commonly treated with cyclosporine,antithymocyte or antilymphocyte globulin, corticosteroids, ora combination of these agents. Fewer than 550 patients weretreated with methotrexate, azathioprine, or monoclonal antibodiesfor acute graft-versus-host disease. Information on drugs usedto treat chronic graft-versus-host disease was incomplete andtherefore not evaluated.
Statistical Analysis
For each transplant recipient, the number of person-years atrisk was calculated from the date of transplantation until thedate of last contact, death, diagnosis of a new cancer, or completionof the study, whichever occurred first. Age-, sex-, year-, andregion-specific incidence rates for all solid cancers combinedand for cancers at specific anatomical sites were applied tothe appropriate person-years at risk to compute the expectednumbers of cancers. Incidence rates for all invasive cancers(except nonmelanoma skin cancers) were obtained from selectedregistries in the United States, England and Wales, Europe,and Asia.10,11,12 Ratios of observed to expected cases and 95percent confidence intervals were calculated on the assumptionthat the observed number of cancers followed a Poisson distribution.13The absolute excess risk was calculated as the observed numberof cancers minus the expected number of cancers per 10,000 transplantrecipients per year. The cumulative probability of a new invasivesolid cancer was estimated by the Kaplan–Meier method.14
Univariate and multivariate analyses were used to compare risksfor various subgroups of transplant recipients who survivedfor at least one year after transplantation, with the use ofPoisson regression methods for grouped survival data13,15 andCox proportional-hazards regression techniques.16 These twoapproaches had nearly identical results, and only the resultsof the Poisson analyses are presented here. Since the risk ofcancer may differ according to the disease for which the transplantationwas performed, the data were stratified according to the primarydisease in six categories: acute lymphoblastic leukemia, acutenonlymphocytic leukemia, chronic myelogenous leukemia, severeaplastic anemia, lymphoma, and other. The data were also stratifiedaccording to the interval since transplantation (with cutoffpoints at 2.5, 5, 7.5, 10, and 12.5 years). Analyses were furtheradjusted for the cohort (Seattle or IBMTR) and the age at thetime of transplantation. Age was entered into the model withthe use of three continuous variables: less than 10, 10 to 39,and 40 or more years. Occurrences of acute graft-versus-hostdisease (grades II to IV) and chronic graft-versus-host disease(moderate or severe disease in the IBMTR cohort and clinicallyextensive disease in the Seattle cohort) were entered as time-dependentcovariates. Except where noted, Poisson regression analyseswere performed for all invasive solid cancers except nonmelanomaskin cancer (71 cases among patients who survived for at leastone year after transplantation); invasive squamous-cell skincancers (8 cases) were considered separately.
Results
Among the 19,229 patients who underwent bone marrow transplantation,80 new cases of invasive solid cancers were observed as comparedwith 29.8 expected cases in the general population (ratio ofobserved to expected cases, 2.7; P<0.001) (Table 2). Therisk of cancer was similar in the IBMTR cohort (observed cases,49; ratio of observed to expected cases, 2.4) and the Seattlecohort (observed cases, 31; ratio of observed to expected cases,3.2). The risks were significantly elevated for cancers of thebuccal cavity (ratio of observed to expected cases, 11.1), liver(7.5), brain and other parts of the central nervous system (7.6),thyroid (6.6), bone (13.4), and connective tissue (8.0) andfor melanoma (5.0). There was little increase in the risk ofcommon adult cancers, such as breast cancer in women or digestive,respiratory, or genitourinary tract cancers in women or men.The overall risk rose steeply over time after transplantation,with a risk that was eight times as high as expected among patientswho survived 10 or more years after transplantation (P for trend,<0.001). The cumulative incidence rate of new solid cancers5, 10, and 15 years after transplantation was 0.7 percent (95percent confidence interval, 0.4 to 0.9 percent), 2.2 percent(95 percent confidence interval, 1.5 to 3.0 percent), and 6.7percent (95 percent confidence interval, 3.7 to 9.6 percent),respectively; the corresponding values for the general populationwere 0.3, 0.6, and 0.8 percent. Only 104 patients were followedfor more than 15 years. The risks of cancers of the buccal cavity,brain, and thyroid tended to be highest five or more years aftertransplantation, whereas the risks of melanoma and cancers ofbone and connective tissue were elevated throughout the follow-upperiod.
Table 2. Ratio of Observed to Expected Cases of New Invasive Solid Cancers According to the Time since Transplantation.
Several unusual cancers were diagnosed. Two of the three livercancers were malignant fibrous histiocytomas, which are extremelyrare in the general population. One patient had Kaposi's sarcomaof the visceral organs (unrelated to the acquired immunodeficiencysyndrome), and one patient had neuroblastoma of the nasal cavities.Bone and connective-tissue cancers included chondrosarcoma (threecases), osteosarcoma (one), rhabdomyosarcoma (two), fibrosarcoma(two), and unspecified bone sarcoma (one). Brain and spinalcord cancers included astrocytoma (four cases), glioblastoma(six), and primitive neuroectodermal cancer (one). Ten of the11 brain cancers developed in patients with acute leukemia.Of the 11 invasive melanomas, 7 occurred in patients with acutenonlymphocytic leukemia; 5 were early-stage lesions (<0.6mm in diameter, Clark level II), 5 were Clark level III or IVlesions (0.9 to 3.8 mm in diameter), and 1 was unclassified.All three salivary gland cancers were mucoepidermoid carcinomas.
Of the 80 patients with new cancers, 36 died. The new cancerwas the primary cause of death in 26 (including 10 with braintumors).
A strong relation was found between the patient's age at thetime of transplantation and the risk of cancer. The risk forchildren who were under 10 years of age at the time of transplantationwas 36.6 times as high as expected; the risk was 4.6 times ashigh as expected for those who were 10 to 29 years old at thetime of transplantation and nearly normal for those who were30 years or older (P for trend, <0.001) (Table 3). The inverseassociation between risk and age persisted when the risk wasevaluated with use of the absolute excess risk (P for trend,0.002). Over half the excess solid tumors in the youngest agegroup were cancers of the brain (observed cases, 9; expectedcases, 0.22) or thyroid (observed cases, 4; expected cases,0.02), with 9 of these 13 tumors occurring in children who hadundergone cranial irradiation before transplantation. When brainand thyroid cancers were excluded from the analysis, there wasno difference in the absolute excess risk among the patientswho were less than 10, 10 to 19, or 20 to 29 years old at thetime of transplantation.
Table 3. Ratio of Observed to Expected Cases and Absolute Excess Risk of New Invasive Solid Cancers According to Age at Transplantation.
The risk of solid cancer also varied according to the primarydisease (Table 4) and tended to be highest for patients withacute leukemia. Significantly elevated risks were also foundfor patients with acute nonlymphocytic leukemia, acute lymphoblasticleukemia, or chronic myelogenous leukemia who had undergonetransplantation before the age of 30 years. Among the patientswho were 30 years or older at the time of transplantation, onlythose with acute nonlymphocytic leukemia had a significantlyincreased risk of solid cancer (ratio of observed to expectedcases, 2.3), and the excess risk of solid tumors for older patientswas similar to that for the patients who underwent transplantationat a younger age (21.0 and 26.6, respectively).
Table 4. Ratio of Observed to Expected Cases and Absolute Excess Risk of New Invasive Solid Cancers According to Age at Transplantation and Primary Disease.
Table 5 shows the results of multivariate regression analysesfor patients who survived for at least one year after transplantation.Ten potential risk factors were evaluated with adjustment forage, time since transplantation, and primary disease (model1 in Table 5). Patients who underwent pretransplantation conditioningwith radiation had an increased risk of cancer as compared withthose who did not receive radiotherapy. The risk of cancer intransplant recipients who underwent limited-field irradiationwas 18.4 times as high as the risk for those who did not undergoirradiation. The doubling of the risk among patients given total-bodyirradiation either as a single dose or in multiple fractionswas not statistically significant. However, the risk increasedsignificantly with increasing doses of radiation for both thepatients who received a single dose and those who received multipledoses (model 2 in Table 5) (P for trend, 0.006 and 0.001, respectively).Among patients undergoing total-body irradiation with a singledose of 10 Gy or higher or fractionated doses totaling 13 Gyor higher, the risk was three to four times that among the patientswho did not undergo irradiation. A similar dose–responsepattern was found when we compared the risk with that in thegeneral population: the ratio of observed to expected caseswas 6.7 for patients receiving a single dose of 10 Gy or higherand 6.1 for those receiving fractionated doses totaling 13 Gyor higher. In these groups, the risk of a new cancer was highestamong the patients who had survived for five or more years (9.3and 14.4, respectively).
Table 5. Multivariate Analysis of Risk Factors for New Invasive Solid Cancers among Patients Who Survived for at Least One Year after Transplantation.
Table 6 shows the results of univariate and multivariate regressionanalyses for individual sites of invasive cancer among the patientssurviving for at least one year after transplantation. Patientswho received high doses of total-body irradiation had a significantincrease in the risk of melanoma and an increased risk of cancerof the brain and thyroid. The risk of buccal cancer was particularlyhigh after limited-field irradiation. Chronic graft-versus-hostdisease was associated with elevated risks of squamous-cellcancers of the buccal cavity and skin. Of the 16 cases in patientswith chronic graft-versus-host disease, 11 occurred in thosewho had received immunosuppressive therapy for two or more years.Twenty-one of the 22 cases of squamous-cell buccal or skin cancerdeveloped in male patients. Depletion of T cells in the donormarrow was associated with a relative risk of invasive melanomaof 4.5 (Table 6) and a relative risk of 5.9 when the two insitu cases and nine invasive cases were considered together(P = 0.02).
Table 6. Risk Factors for New Invasive Solid Cancers among Patients Who Survived for at Least One Year after Transplantation, According to the Site of Cancer.
The immunosuppressive drugs used to prevent or treat acute graft-versus-hostdisease had no apparent effect on the risk of a new solid cancerin univariate or multivariate analyses. The drugs used for pretransplantationconditioning, evaluated singly and in combination, were notsignificantly related to the risk of solid cancer.
Discussion
Our analysis of nearly 20,000 bone marrow recipients, including3200 who survived for five or more years, revealed a high riskof specific solid cancers after transplantation. The risk increasedsharply over time (to 6.7 percent at 15 years) and was highestamong children who had undergone transplantation when they wereless than 10 years old. Statistically significant increasesin risk were confined to melanoma and cancers of the buccalcavity, brain, liver, thyroid, bone, and connective tissue.The increased risk of new solid cancers after bone marrow transplantationis likely to be related to pretransplantation conditioning withradiation, altered immune function, and prior treatment forthe primary disease.
Previous studies have reported an increased incidence of newcancers after bone marrow transplantation, mainly lymphomasand hematopoietic disorders, which occurred early in the follow-upperiod.2,4,5,6,7,17,18,19 Lymphoproliferative disorders arethe most common cancer in the first year after allogeneic bonemarrow transplantation; most are related to compromised immunefunction and Epstein–Barr virus infection.2,7 The estimated10-year cumulative incidence of lymphoma in our cohort is lessthan 1.5 percent, with no cases of lymphoma observed 10 or moreyears after transplantation.
Data on post-transplantation solid cancers are sparse. The twolargest studies reported small numbers of cancers at individualanatomical sites and an overall risk that was two to three timesas high as that in the general population.2,7 Studies in animalshave also linked various solid tumors to bone marrow transplantation.18,20
Whole-body irradiation at the doses typically given to transplantrecipients would be fatal without bone marrow transplantation.The transplantation experience is also unique because largedoses of radiation are given to patients who will also haveimpaired immune function. In our study, the risk of a solidcancer among patients who survived for one or more years aftertransplantation rose with the dose of radiation, with threeto four times the risk at the highest dose levels, as comparedwith those who did not receive radiation therapy. The elevatedrisks for several solid cancers are consistent with a radiogeniceffect, especially for cancers of the thyroid, salivary gland,bone, connective tissue, and brain.21 The 18-fold risk of cancerin patients who received limited-field irradiation is almostentirely attributable to a higher-than-expected number of cancersafter thoracoabdominal irradiation among patients with severeaplastic anemia who were treated at a single center, as reportedpreviously.6,22
Radiogenic cancers generally have a long latent period, andthe risk of such cancers is frequently high among patients undergoingirradiation at a young age.21,23 Transplant recipients routinelyundergo thorough follow-up examinations, which may result inearly detection of secondary cancers. We found that young childrengiven radiotherapy as part of the conditioning regimen had ahigh risk of cancer of the brain or thyroid, and most of thesepatients had received cranial irradiation before transplantation.Radiogenic thyroid cancer has been reported in children exposedto high or low doses of radiation but not in adults.24,25 Higherthan expected numbers of brain cancers have been reported amongchildren treated with cranial irradiation at doses of 1 to 3Gy for tinea capitis26 and 18 to 24 Gy for acute lymphoblasticleukemia.27
Studies of patients who were exposed to radiation have foundincreased risks of bone and connective-tissue cancers in thesepatients only when the radiation doses surpassed 10 Gy.28,29,30We found an increased risk of salivary gland cancer after radiationtherapy — three cases — which is consistent withthe strong dose response of the mucoepidermoid carcinomas ofthe salivary gland reported among survivors of the atomic bomb.31
Patients with immunodeficiency diseases and those receivingimmunosuppressive therapy for organ transplants are prone tothe development of cancer at certain sites.32,33,34 We foundno link between immune dysfunction (i.e., HLA-mismatched marrowtransplants, T-cell depletion, or graft-versus-host disease)and an elevated risk of solid cancer (all types combined), norcould we confirm an excess risk associated with the administrationof antithymocyte globulin for graft-versus-host disease.3 However,the large increase in the risk of melanoma in our study andthe possible association of melanoma with T-cell depletion areconsistent with the findings in immunosuppressed patients withrenal allografts35 or malignant lymphoma.36,37 The mechanismof the association between melanoma and high doses of radiationis unclear, since melanoma has not previously been linked toionizing radiation.21,23 Immunologic factors may also contributeto the increased risk of squamous-cell skin cancers after bonemarrow or renal transplantation, especially in regions whereone can be exposed to strong sunlight.33 Immunologic alterationsmay predispose patients to squamous-cell cancers of the buccalcavity, particularly in view of the association between oralmucositis and chronic graft-versus-host disease. A recent studyof patients with aplastic anemia who underwent transplantationat the Fred Hutchinson Cancer Research Center in Seattle orHôpital St. Louis in Paris showed that the incidence ofsolid tumors, predominantly tumors of the buccal cavity andskin, was significantly increased after the administration ofazathioprine for chronic graft-versus-host disease.4 In immunosuppressedpatients, oncogenic viruses such as human papillomaviruses maycontribute to squamous-cell cancers of the skin and buccal mucosaafter transplantation.32,38 The excess risk of squamous-cellcancers of the buccal cavity and skin among male patients isunexplained, but it may indicate an interaction between ionizingradiation, immunodeficiency, and other risk factors more prevalentamong men than women.
In our study, only 690 transplant recipients were followed for10 or more years, which limited our ability to estimate therisk of cancer among long-term survivors. Follow-up of recipientssurviving 10 to 20 years after transplantation should clarifythe risks of breast, lung, and other cancers that may ariseonly after a long latent period. The experience of patientswith Hodgkin's disease and others who underwent irradiationat a young age21,23,39,40 indicates that the risk of canceramong patients who receive transplants at a young age and surviveto adulthood may be even higher than that reported in our study.
Bone marrow transplantation prolongs survival or is curativein many patients with cancer or other life-threatening diseases.These benefits clearly outweigh the risks of late complications.However, our results should alert physicians that recipientsof bone marrow transplants, particularly those receiving transplantsat a young age, have an increased incidence of new solid cancersand that the excess risk of cancer rises sharply with time.Transplant recipients should be followed indefinitely to detectearly cancer and precursor lesions (e.g., dysplastic nevi, actinickeratoses, and oral leukoplakia), and they should avoid carcinogenicexposures (e.g., exposure to tobacco), which may potentiatethe risk of solid cancers.
Supported by contracts (CP-21161 and CP-21103) with and grants(P01-CA-18029, P01-CA-47748, P01-CA-18221, and P01-CA-15704)from the National Cancer Institute; a Public Health Servicegrant (P01-CA-40053) from the National Cancer Institute, theNational Institute of Allergy and Infectious Diseases, and theNational Heart, Lung, and Blood Institute; a grant (P01-HL-36444)from the National Heart, Lung, and Blood Institute; and by grantsfrom the following: Alpha Therapeutic Corporation; Amgen, Inc.;Applied Immune Services; Amour Pharmaceutical Company; AstraPharmaceutical; Baxter HealthCare Corporation; Bayer Corporation;Biogen; Blue Cross and Blue Shield Association; Lynde and HarryBradley Foundation; Bristol-Myers Squibb Company; Frank G. BrotzFamily Foundation; Center for Advanced Studies in Leukemia;Charles E. Culpeper Foundation; Eleanor Naylor Dana CharitableTrust; Eppley Foundation for Research; Genentech, Inc.; GlaxoWellcome Company; Hoechst Marion Roussel, Inc.; Immunex Corporation;Kettering Family Foundation; Kirin Brewery Company; Robert J.Kleberg, Jr., and Helen C. Kleberg Foundation; Herbert H. KohlCharities, Inc.; Eli Lilly Company Foundation; Nada and HerbertP. Mahler Charities; Milstein Family Foundation; Milwaukee Foundation/ElsaSchoeneich Research Fund; Samuel Roberts Noble Foundation; OrthoBiotech Corporation; John Oster Family Foundation; Elsa U. PardeeFoundation; Jane and Lloyd Pettit Foundation; Pfizer, Inc.;Pharmacia; RGK Foundation; Sandoz Pharmaceuticals; Schering–PloughInternational; Walter Schroeder Foundation; Stackner FamilyFoundation; Starr Foundation; Joan and Jack Stein Charities;and Wyeth–Ayerst Laboratories.
We are indebted to all the investigators and staff at the participatingtransplantation centers who contributed data to this study;to Keith Sullivan, Mary Flowers, Jean Sanders, and Ted Gooleyat the Fred Hutchinson Cancer Research Center for their continuoussupport of the study; to Muriel Siadek, Kathy Erne, Janet Nims,Mariann Hansen, and Linda Glockling at the Fred Hutchinson CancerResearch Center and Sharon K. Nell and Diane Knutsen at theIBMTR for support in collecting data; to Kathy Chimes, ElenaAdrianza, and Diane Fuchs from Westat Inc. for coordinationof field studies; and to George Geise and Dennis Buckman fromInformation Management Services for computing support.
Source Information
From the Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, Md. (R.E.C., D.A.S., L.B.T., R.N.H., J.F.F., J.D.B.); the International Bone Marrow Transplant Registry, Medical College of Wisconsin, Milwaukee (P.A.R., M.M.H., K.A.S.); the Fred Hutchinson Cancer Research Center, Seattle (H.J.D., R.P.W.); and Hôpital Saint Louis, Hématologie–Greffe de Moelle, Paris (G.S.). Other authors were H. Gary Schoch, B.A., George E. Sale, M.D., and Rainer Storb, M.D. (Fred Hutchinson Cancer Research Center, Seattle); William D. Travis, M.D. (Armed Forces Institute of Pathology, Washington, D.C.); Hans-Jochem Kolb, M.D. (University of Munich, Munich, Germany); Robert Peter Gale, M.D., Ph.D. (Salick Health Care, Los Angeles); and Jakob R. Passweg, M.D. (International Bone Marrow Transplant Registry, Milwaukee).
Address reprint requests to Ms. Curtis at Executive Plaza North, Suite 408, National Cancer Institute, Bethesda, MD 20892.
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(2008). Old and New Cancers after Hematopoietic-Cell Transplantation. ASH Education Book
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Epstein, J. B., Gorsky, M., Fischer, D., Gupta, A., Epstein, M., Elad, S.
(2007). A Survey of the Current Approaches to Diagnosis and Management of Oral Premalignant Lesions. Journal of the American Dental Association
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Nash, R. A., McSweeney, P. A., Crofford, L. J., Abidi, M., Chen, C.-S., Godwin, J. D., Gooley, T. A., Holmberg, L., Henstorf, G., LeMaistre, C. F., Mayes, M. D., McDonagh, K. T., McLaughlin, B., Molitor, J. A., Nelson, J. L., Shulman, H., Storb, R., Viganego, F., Wener, M. H., Seibold, J. R., Sullivan, K. M., Furst, D. E.
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Cogle, C. R., Theise, N. D., Fu, D., Ucar, D., Lee, S., Guthrie, S. M., Lonergan, J., Rybka, W., Krause, D. S., Scott, E. W.
(2007). Bone Marrow Contributes to Epithelial Cancers in Mice and Humans as Developmental Mimicry. Stem Cells
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Cohen, A., Rovelli, A., Merlo, D. F., van Lint, M. T., Lanino, E., Bresters, D., Ceppi, M., Bocchini, V., Tichelli, A., Socie, G.
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(2006). Keratinocyte growth factor expression and activity in cancer: implications for use in patients with solid tumors.. JNCI J Natl Cancer Inst
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(2006). Nonmelanoma Skin and Mucosal Cancers After Hematopoietic Cell Transplantation. JCO
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(2005). Preliminary Results of the Safety of Immunotherapy with Gemtuzumab Ozogamicin following Reduced Intensity Allogeneic Stem Cell Transplant in Children with CD33+ Acute Myeloid Leukemia. Clin. Cancer Res.
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(2005). New approaches for preventing and treating chronic graft-versus-host disease. Blood
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Tichelli, A., Socie, G.
(2005). Considerations for Adult Cancer Survivors. ASH Education Book
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(2005). Hematopoietic stem cell transplantation (HSCT) in children with juvenile myelomonocytic leukemia (JMML): results of the EWOG-MDS/EBMT trial. Blood
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(2004). Long-Term Follow-Up of Thyroid Function in Patients Who Received Bone Marrow Transplantation during Childhood and Adolescence. J. Clin. Endocrinol. Metab.
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(2004). Hematopoietic stem cell transplantation: a primer for the primary care physician. CMAJ
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(2003). Incidence of Non-AIDS-Defining Cancers Before and During the Highly Active Antiretroviral Therapy Era in a Cohort of Human Immunodeficiency Virus-Infected Patients. JCO
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(2003). Ongoing Care of Patients After Primary Treatment for Their Cancer. CA Cancer J Clin
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Baker, K. S., DeFor, T. E., Burns, L. J., Ramsay, N. K.C., Neglia, J. P., Robison, L. L.
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(2003). Factors influencing outcome and incidence of long-term complications in children who underwent autologous stem cell transplantation for acute myeloid leukemia in first complete remission. Blood
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(2001). Hematopoietic cell transplantation in older patients with hematologic malignancies: replacing high-dose cytotoxic therapy with graft-versus-tumor effects. Blood
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(2001). MRI and CSF oligoclonal bands after autologous hematopoietic stem cell transplantation in MS. Neurology
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Bhatia, S., Louie, A. D., Bhatia, R., O'Donnell, M. R., Fung, H., Kashyap, A., Krishnan, A., Molina, A., Nademanee, A., Niland, J. C., Parker, P. A., Snyder, D. S., Spielberger, R., Stein, A., Forman, S. J.
(2001). Solid Cancers After Bone Marrow Transplantation. JCO
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Kluin-Nelemans, H. C., Zagonel, V., Anastasopoulou, A., Bron, D., Roozendaal, K. J., Noordijk, E. M., Musson, H., Teodorovic, I., Maes, B., Carbone, A., Carde, P., Thomas, J.
(2001). Standard Chemotherapy With or Without High-Dose Chemotherapy for Aggressive Non-Hodgkin's Lymphoma: Randomized Phase III EORTC Study. JNCI J Natl Cancer Inst
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Knollmann, F. D., Hummel, M., Hetzer, R., Felix, R.
(2000). CT of Heart Transplant Recipients: Spectrum of Disease. RadioGraphics
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(2000). Unrelated donor marrow transplantation for chronic myelogenous leukemia: 9 years' experience of the National Marrow Donor Program. Blood
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(2000). New Malignant Diseases After Allogeneic Marrow Transplantation for Childhood Acute Leukemia. JCO
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Young, N. S., Abkowitz, J. L., Luzzatto, L.
(2000). New Insights into the Pathophysiology of Acquired Cytopenias. ASH Education Book
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Kolb, H. J., Socie, G., Duell, T., Van Lint, M. T., Tichelli, A., Apperley, J. F., Nekolla, E., Ljungman, P., Jacobsen, N., van Weel, M., Wick, R., Weiss, M., Prentice, H. G., for the Late Effects Working Party of the European,
(1999). Malignant Neoplasms in Long-Term Survivors of Bone Marrow Transplantation. ANN INTERN MED
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(1999). Risk of Lymphoproliferative Disorders After Bone Marrow Transplantation: A Multi-Institutional Study. Blood
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(1999). An Evidence-Based Analysis of the Effect of Busulfan, Hydroxyurea, Interferon, and Allogeneic Bone Marrow Transplantation in Treating the Chronic Phase of Chronic Myeloid Leukemia: Developed for the American Society of Hematology. Blood
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Young, N. S.
(1999). Acquired Aplastic Anemia. JAMA
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(1999). Long-Term Survival and Late Deaths after Allogeneic Bone Marrow Transplantation. NEJM
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Thomas, E. D.
(1999). Does Bone Marrow Transplantation Confer a Normal Life Span?. NEJM
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Cohen, A., Rovelli, A., Bakker, B., Uderzo, C., van Lint, M.-T., Esperou, H., Gaiero, A., Leiper, A. D., Dopfer, R., Cahn, J. Y., Merlo, F., Kolb, H. J., Socie, G.
(1999). Final Height of Patients Who Underwent Bone Marrow Transplantation for Hematological Disorders During Childhood: A Study by the Working Party for Late Effects-EBMT. Blood
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(1999). Cirrhosis of the Liver in Long-Term Marrow Transplant Survivors. Blood
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(1999). Telomere Stability Is Frequently Impaired in High-Risk Groups of Patients with Myelodysplastic Syndromes. Clin. Cancer Res.
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(1999). Increased Risk of Chronic Graft-Versus-Host Disease, Obstructive Bronchiolitis, and Alopecia With Busulfan Versus Total Body Irradiation: Long-Term Results of a Randomized Trial in Allogeneic Marrow Recipients With Leukemia. Blood
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Parisi, M. T., Fahmy, J. L., Kaminsky, C. K., Malogolowkin, M. H.
(1999). Complications of Cancer Therapy in Children: A Radiologist's Guide. RadioGraphics
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(1999). Problems in Hodgkin's Disease Management. Blood
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(1998). Malignancies After Hematopoietic Stem Cell Transplantation: Many Questions, Some Answers. Blood
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(1997). Solid Cancers after Bone Marrow Transplantation. NEJM
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