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Ethnic differences in chronic health conditions after hematopoietic cell transplantation†
A report from the Bone Marrow Transplant Survivor Study
Article first published online: 19 AUG 2010
Copyright © 2010 American Cancer Society
Volume 116, Issue 17, pages 4152–4159, 1 September 2010
How to Cite
Armenian, S. H., Sun, C.-L., Teh, J. B., Arora, M., Baker, K. S., Francisco, L., Forman, S. J. and Bhatia, S. (2010), Ethnic differences in chronic health conditions after hematopoietic cell transplantation. Cancer, 116: 4152–4159. doi: 10.1002/cncr.25157
Presented in part at the 50th Annual Meeting of the American Society of Hematology, San Francisco, California, December 6-9, 2008.
- Issue published online: 23 AUG 2010
- Article first published online: 19 AUG 2010
- Manuscript Accepted: 17 NOV 2009
- Manuscript Revised: 11 NOV 2009
- Manuscript Received: 10 OCT 2009
- chronic health conditions;
- graft-versus-host disease;
- health insurance coverage;
- health-related outcomes;
- hematologic malignancies;
- sociodemographic factors
Hispanics have a greater risk of early treatment failure after hematopoietic stem cell transplantation (HCT) compared with non-Hispanic whites. However, long-term morbidity among Hispanics has not been described.
Health-related outcomes were examined in 159 Hispanic patients and 825 non-Hispanic white patients who underwent HCT between 1974 and 1998 and survived a mean of 8.7 years. Patients completed a detailed questionnaire about sociodemographic factors and the occurrence of chronic health conditions.
Exposure to total body irradiation (TBI) (odds ratio [OR], 1.94; 95% confidence interval [CI], 1.06-3.56; P = .03), the presence of chronic graft versus host disease (GvHD) (OR, 3.99; 95% CI, 1.94-8.24; P = .002), and health insurance coverage (OR, 3.46; 95% CI, 1.5-8.01; P = .004), were associated significantly with severe/life-threatening conditions. Compared with non-Hispanic white patients, Hispanic patients were 53% less likely to report severe/life-threatening conditions (OR, 0.47; 95% CI, 0.27-0.83; P = .009) after adjusting for relevant clinical variables. This effect size was mitigated (OR, 0.56; 95%CI, 0.29-1.08; P = .08) after adjusting for health insurance coverage.
Hispanics were less likely to report severe/life-threatening health conditions after HCT than non-Hispanic whites—a difference that decreased in magnitude and significance after taking health insurance into consideration. Although the current results confirmed the role of TBI and chronic GvHD, in the current study, the role of a lack of health insurance coverage was identified as a mediator of the lower prevalence of self-reported long-term morbidity in Hispanics. Cancer 2010. © 2010 American Cancer Society.
Hematopoietic cell transplantation (HCT) has become the treatment of choice for several life-threatening disorders.1, 2 Improvements in transplantation strategies have contributed to increments in survival rates of 10% per decade.3 Patients with hematologic malignancies who survive for 2 years after HCT have 10-year survival rates that exceed 70%.4-6 However, these improvements are not enjoyed equally by all. Data from the Center for International Blood and Marrow Transplant Research (CIBMTR) demonstrate that Hispanics are at a greater risk for early events, such as treatment-related mortality (TRM) or disease recurrence, compared with white non-Hispanics who undergo allogeneic HCT.7, 8 Conversely, the Bone Marrow Transplant Survivor Study (BMTSS) has not identified ethnic/racial differences in late nonrecurrence-related mortality after autologous5 or allogeneic HCT.6
The Institute of Medicine (IOM) Report on Race and Unequal Treatment9 considers Hispanics to be a vulnerable population for adverse health-related outcomes because of socioeconomic and cultural issues that could create barriers to access to the healthcare system. Although they are the largest minority group in the United States (14.4% of the US population) and the fastest growing (projected 29% of the US population by 2050),10 the IOM Report indicates that Hispanics are under represented disproportionately in studies that examine barriers to healthcare access and disparities in health-related outcomes. Indeed, there exists a paucity of data regarding the long-term burden of morbidity that are unique to Hispanic HCT survivors.
In a previous report, we demonstrated that Hispanic HCT survivors are more likely to be uninsured and to have lower family income and education, and they are significantly less likely to establish contact with primary care providers after HCT.11 The objectives of the current study were to describe the burden of morbidity reported by long-term Hispanic HCT survivors compared with their white, non-Hispanic counterparts and to examine the role of sociodemographic factors to explain the observed differences.
MATERIALS AND METHODS
The BMTSS is a collaboration between the City of Hope National Medical Center (COH) and the University of Minnesota (UMN). Its objective is to examine the long-term outcomes of individuals who have survived for >2 years after HCT. Eligible participants include individuals who underwent HCT at COH or UMN between 1974 and 1998 for a hematologic malignancy or for severe aplastic anemia (SAA), who survived for >2 years after transplantation, who were alive and aged ≥18 years at the time of study participation, and who identified themselves as Hispanic or non-Hispanic white. The Human Subjects Protection Committees at the participating institutions approved the study. Informed consent was obtained according to the Declaration of Helsinki.
Information regarding primary diagnoses, preparative regimens, stem cell sources (autologous or allogeneic), risk of recurrence at HCT (standard vs high risk), and management of chronic graft versus host disease (GvHD) was obtained from institutional transplantation databases. Patients who underwent transplantation in first or second complete remission after acute leukemia (acute myeloid or lymphoid leukemia) and lymphoma (Hodgkin or non-Hodgkin lymphoma) or in first chronic phase of chronic myeloid leukemia and all patients with SAA were considered to be at standard risk of recurrence. All other patients were considered to be at high risk of recurrence.
A 255-item mailed questionnaire (available in English and Spanish) was used to collect information from all participants who were alive at the time of study enrollment and covered the following general areas: sociodemographics (race/ethnicity, marital status, education, employment, annual household income, and health insurance), the use of medical care over the previous 2 years, the presence of chronic GvHD, and a diagnosis of physical health conditions with age at diagnosis (endocrinopathies, central nervous system compromise, cardiopulmonary dysfunction, gastrointestinal and hepatic sequelae, musculoskeletal abnormalities, and subsequent malignancies). An individual was considered to have active chronic GvHD if they reported active management of their chronic GvHD at the time of study participation or within 12 months of study participation. The reliability and validity of the BMTSS questionnaire has been tested, and the results indicate moderate to high agreement between self-reported outcomes and medical records.12
Both the Spanish and English versions of the BMTSS questionnaire were mailed to individuals with a Spanish surname, and bilingual instructions were included to complete the questionnaire in the language of their preference. A follow-up telephone call was made to all study participants (irrespective of race/ethnicity) by a bilingual interviewer to confirm the language of preference and to address any concerns or questions regarding the study in the appropriate language. If the need for a Spanish version of the questionnaire was identified during the call (if only the English version had been mailed initially), then the Spanish version was mailed.
Chronic Health Conditions
All chronic health conditions that were diagnosed after HCT were graded using the Common Terminology Criteria for Adverse Events, version 3.0 (CTCAEv3.0), a scoring system that was developed through the National Cancer Institute by a multidisciplinary group13. The CTCAEv3.0 is used to grade acute and chronic conditions in patients with cancer and cancer survivors and distinguishes grades 1 through 5 with unique clinical descriptions of the severity for each event (grade 1, mild toxicity; grade 2, moderate toxicity; grade 3, severe toxicity; grade 4, life-threatening/disabling toxicity; and grade 5, adverse event-related death). Gonadal dysfunction and psychosocial outcomes were not included in the current analysis. This scoring system was adapted from the system used by the Childhood Cancer Survivor Study14 with the addition of complications that are unique to the HCT population (such as avascular necrosis, dry eye, dry mouth, bleeding, or swelling gums).
The prevalence of chronic health conditions was determined for participating HCT survivors. Chronic health conditions were reported as the presence of any condition (grades 1 through 4) and were dichotomized as mild to moderate (grades 1 and 2) or severe/life-threatening/disabling (grades 3 and 4). For participants who had more than 1 condition, the maximum grade was used in the analysis. Descriptive statistics were calculated using standard parametric and nonparametric tests. Multivariate logistic regression analysis was used to identify variables that were associated with the development of severe/life-threatening/disabling (grades 3 or 4) chronic health conditions after HCT (dependent variable). In addition to the primary independent variable of interest (ethnicity), other variables in Model 1 included those with a biologic basis for association with health conditions (sex, age at study participation, primary diagnosis, year of transplantation, source of stem cells, exposure to total body irradiation [TBI], and the presence of active chronic GvHD). This was followed by the introduction of education and health insurance status into the model (Model 2) to help explain any association between ethnicity and health conditions identified in Model 1. The results were reported as odds ratios (ORs) with 95% confidence intervals (CIs).
The cumulative incidence of chronic health conditions was calculated for Hispanic and non-Hispanic white HCT recipients using competing risk methods.15 This analysis included patients who had undergone HCT and survived for ≥2 years (including 519 patients who subsequently died). Cause of death information was obtained from medical records and from the National Death Index.5, 6 Deaths caused by chronic health conditions (n = 217) were considered grade 5; deaths from primary disease/accident/suicide (n = 302) were considered as deaths from competing risk. It was assumed that nonparticipants had no chronic health conditions, and follow-up was censored at the date of last contact available from the institutional databases to provide a conservative estimate of the cumulative incidence. Data were analyzed using the SAS 9.1 software package (SAS Institute, Cary, NC). All statistical tests were 2-sided.
Of the 1571 eligible patients, 1414 patients (90%) were contacted successfully, and, of these, 984 patients (70%) agreed to participate, including 159 Hispanics (116 English-speaking and 43 Spanish-speaking) and 825 non-Hispanic whites. Participants were more likely to be women (44.6% vs 38.7%; P = .02), to be older at the time of HCT (aged 34.7 years vs 29.3 years; P < .01) and at study participation (aged 43.4 years vs 39.8 years; P < .01), to have shorter follow-up after HCT (mean follow-up, 8.7 years vs 10.5 years; P < .01), to be more likely to have undergone autologous transplantation (45% vs 37%; P = .002), and to have received TBI (77% vs 69.7; P < .01). Hispanics were significantly less likely to participate (61%) compared with non-Hispanic whites (71%; P < .01). Patients who had undergone HCT for SAA were less likely to participate compared with survivors who had other diagnoses. The participation rate did not differ by risk of recurrence at HCT or by transplanting institution.
Characteristics of the study participants are presented in Table 1. The mean age at study participation was 41.5 years (range, 20.0-67.4 years) for Hispanics and 43.8 years (range, 18.2-73.0 years) for non-Hispanic whites (P = .02), and the mean follow-up was 9.0 years (range, 2.5-25.2 years) and 8.7 years (range, 2.0-27.8 years; P = .45), respectively. Hispanics were significantly less likely to have completed high school (45.9% vs 96.3%; P < .01) and to have health insurance coverage (75.5% vs 93.7%; P < .01). Hispanic study participants were significantly more likely to have undergone allogeneic HCT (67.9% vs 52.5%; P < .01). Hispanic survivors had a higher prevalence of acute leukemia (42.1% vs 32.4%) but a lower prevalence of lymphoma (17.6% vs 31.3%) compared with non-Hispanic whites. There were no differences with respect to sex, exposure to TBI, or the presence of active chronic GvHD.
|Characteristic||No. of Patients (%)||P|
|Non-Hispanic White, N=825||Hispanic, N=159,|
|Age: Mean±SD, y|
|At study participation||43.8±12.2||41.5±11.0||.03|
|Men||448 (54.3)||97 (61)||.12|
|Married||510 (61.8)||89 (55.9)||.17|
|<High school||28 (3.4)||86 (54)|
|Completed high school||797 (96.6)||73 (45.9)||<.01|
|Currently insured||773 (93.7)||120 (75.5)||<.01|
|Lymphoma||258 (31.3)||28 (17.6)|
|Non-Hodgkin lymphoma||181 (21.9)||18 (11.3)|
|Hodgkin lymphoma||77 (9.3)||10 (6.3)|
|Acute leukemia||267 (32.4)||67 (42.1)|
|Acute lymphatic leukemia||71 (8.6)||24 (15.1)|
|Acute myeloid leukemia||196 (23.8)||43 (27)||<.01|
|Chronic myeloid leukemia||190 (23)||39 (24.5)|
|Other||110 (13.3)||25 (15.7)|
|Severe aplastic anemia||35 (4.2)||13 (8.2)|
|Multiple myeloma||30 (3.6)||10 (6.3)|
|Other||45 (5.5||2 (1.3)|
|Allogeneic transplantation||433 (52.5)||108 (67.9)||<.01|
|Total body irradiation||635 (77)||121 (76.1)||.88|
|Risk of recurrence at HCT|
|High risk||295 (35.9)||52 (32.7)||.44|
|BMI: Mean±SD, kg/m2|
|Year of transplantation|
|≤1985||103 (12.5)||21 (13.2)|
|1986 to 1990||134 (16.2)||25 (15.7)|
|1991 to 1995||305 (37)||65 (40.9)|
|≥1996||283 (34.3)||48 (30.2)||.73|
Hispanics were significantly less likely to report a chronic health condition of any severity (57.2% vs 69.1%; P < .01) and of grade 3 or 4 severity (16.4% vs 19.6%; P = .04) or to report multiple (≥2) health conditions (43.4% vs 51.9%; P = .05) compared with non-Hispanic whites (Table 2). Commonly occurring grade 3 or 4 health conditions for the entire study population included gastrointestinal complications (10.7%), musculoskeletal complications (10.1%), audiovisual impairment (8.5%), and second malignant neoplasms (7.6%). The prevalence of the specific types of chronic health conditions reported by Hispanics and non-Hispanic whites did not differ.
|Chronic Condition||No. of Patients (%)||P|
|Non-Hispanic White, N=825||Hispanic, N=159|
|No condition||255 (30.9)||68 (42.8)|
|Grade 1, mild||123 (14.9)||21 (13.2)|
|Grade 2, moderate||285 (34.6)||44 (27.7)||.08|
|Grade 3, severe||123 (14.9)||20 (12.6)|
|Grade 4, life threatening/disabling||39 (4.7)||6 (3.8)|
|Grades 1-4||570 (69.1)||91 (57.2)||<.01|
|Grades 3 or 4||162 (19.6)||26 (16.4)||.04|
|Multiple health conditions|
|≥2||428 (51.9)||69 (43.4)||.05|
|≥3||293 (35.5)||51 (32.1)||.40|
Multivariate analysis (Table 3) revealed that Hispanics were less likely to report a grade 3 or 4 health condition compared with non-Hispanic whites (OR, 0.47; 95% CI, 0.27-0.83; P = .009) in Model 1, which did not contain education, and health insurance status. The introduction of those sociodemographic variables diminished both the magnitude and the significance of the association between ethnicity and health conditions (OR, 0.56; 95% CI, 0.29-1.08; P = .08).
|Risk Factor||Model 1||Model 2|
|OR (95% CI)||P||OR (95% CI)||P|
|Women||1.18 (0.79-1.77)||.41||1.15 (0.76-1.73)||.51|
|At HCT||0.88 (0.81-0.96)||.004||0.88 (0.80-0.96)||.003|
|At study participation||1.17 (1.07-1.27)||.0007||1.17 (1.07-1.27)||.0008|
|Hispanic||0.47 (0.27-0.83)||.009||0.56 (0.29-1.08)||.08|
|Chronic myeloid leukemia||0.70 (0.30-1.65)||.41||0.65 (0.27-1.54)||.32|
|Acute leukemia||0.95 (0.44-2.08)||.90||0.93 (0.42-2.06)||.85|
|Lymphoma||1.02 (0.47-2.23)||.95||0.94 (0.43-2.07)||.88|
|Type of transplantation|
|Allogeneic, no active chronic GvHD||1.13 (0.63-2.06)||.68||1.17 (0.64-2.15)||.61|
|Allogeneic, active chronic GvHD||4.01 (1.97-8.14)||.001||3.99 (1.94-8.24)||.002|
|Chemotherapy and TBI||1.81 (0.99-3.29)||.05||1.94 (1.06-3.56)||.03|
|Year of transplantation|
|1991 to 1995||1.21 (0.54-2.67)||.64||1.23 (0.55-2.77)||.61|
|≥1996||0.91 (0.31-2.72)||.87||0.92 (0.30-2.81)||.89|
|Completed high school||0.98 (0.45-2.12)||.95|
Other variables that were associated with an increased reporting of grade 3 or 4 chronic health conditions included the presence of active chronic GvHD (OR, 3.99; 95% CI, 1.94-8.24; P = .002), health insurance coverage (OR, 3.46; 95% CI, 1.5-8.01; P = .004), and exposure to TBI (OR, 1.94; 95%CI, 1.06-3.56; P = .03). Individuals with active chronic GvHD were significantly more likely to report grade 3 or 4 audiovisual impairment (25% vs 9.1%; P = .04), endocrinopathies (25% vs 7.7%; P = .03), and gastrointestinal complications (28% vs 9.1%; P = .02) compared with other allogeneic HCT recipients who did not have active chronic GvHD. Participants who received TBI were significantly more likely to report grade 3 or 4 musculoskeletal complications (12.8% vs 3.1%; P = .01) or gastrointestinal complications (10.9% vs 3.1%; P = .03) compared with participants who were not exposed to TBI.
The cumulative incidence of chronic health conditions among Hispanics and non-Hispanic whites was 35% (95% CI, 30%-40%) and 43% (95% CI, 41%-46%) at 10 years after HCT, respectively (P < .01) (Fig. 1). Corresponding estimates for grade 3 or 4 chronic health conditions were 8% (95% CI, 5%-11%) and 10% (95% CI, 8%-11%), respectively; and the estimates for grade 5 chronic health conditions were 11% (95% CI, 8%-15%) and 14% (95% CI, 12%-16%), respectively.
The overall objective of this study was to determine whether ethnic differences existed in the prevalence of chronic health conditions after HCT. Although the CIBMTR report indicated that Hispanics had a 30% increased risk of early post-HCT events,7 other investigators failed to replicate those findings and suggested that the differences in outcome may be less about ethnicity and more about socioeconomic status and the barriers to healthcare access faced by these populations.16 Furthermore, in previous reports, BMTSS identified no ethnic/racial differences in late mortality from causes unrelated to disease recurrence.5, 6
There is a paucity of data regarding the magnitude of long-term morbidity in Hispanic HCT survivors, whether there are differences in morbidity between non-Hispanic whites and Hispanics, and the possible causes of these differences. In the current study, we observed that Hispanics were 53% less likely to report chronic severe/life-threatening/disabling conditions compared with non-Hispanic whites after adjusting for relevant clinical variables—an effect size that was mitigated after adjusting for known sociodemographic factors, most notably, health insurance coverage.
The availability of health insurance determines the timeliness and quality of healthcare received by survivors.9 Hispanics face greater barriers to health insurance access than all other racial/ethnic groups, which makes them less likely to have a regular source of care.9, 17, 18 The prevalence of being uninsured among Hispanics is 33% compared with 17% for the general population.9, 19 The current study indicated that Hispanics were significantly more likely to be uninsured at study participation (24.5%) compared with non-Hispanic whites (6.3%). Those who had health insurance coverage were 3-fold more likely to report a severe/life-threatening condition independent of other modifying risk factors, such as socioeconomic status, age, sex, and treatment-related conditions. In fact, having health insurance coverage was associated with a greater likelihood of the diagnosis and reporting of severe/life-threatening/disabling health conditions after HCT in both Hispanics and non-Hispanic whites. There are several reasons why having health insurance would increase the likelihood of reporting chronic health conditions: First, as reported by others, long-term cancer survivors who have health insurance are more likely to undergo recommended health-related screenings, such as echocardiograms, mammograms, and Papanicolaou smears, thus increasing the likelihood of detection of the condition being screened.20-22 In fact, in a previous study, we demonstrated that lack of health insurance is associated with a lower prevalence of healthcare use by this cohort of HCT survivors.11 Second, the availability of health-related resources and access to healthcare presumably would lead to an improvement in health-related knowledge, enabling these survivors to characterize more accurately the nature and severity of their chronic medical conditions.23, 24
The paucity of information regarding these barriers in previous studies probably is because relatively small numbers of Hispanics have been included in studies evaluating long-term outcomes after HCT.7, 16 For example, it is recognized increasingly that language proficiency plays an important role in health-related knowledge and access to primary care.9, 25, 26 With nearly 30% of Hispanics in the United States currently living in a linguistically isolated household,10 language proficiency is likely to play an increasingly important role in the design of studies that evaluate long-term outcomes in these at-risk populations. These issues need to be addressed comprehensively to develop support systems and informed interventions for the vulnerable subpopulations, as highlighted in the recent American Society of Clinical Oncology Policy Statement on Disparities in Cancer Care.27
We also demonstrated that the presence of active chronic GvHD increases the risk of chronic severe/life-threatening/disabling conditions. Chronic GvHD is a leading cause of nonrecurrence-related mortality and is associated with chronic renal toxicity, musculoskeletal abnormalities, cardiopulmonary compromise, and gastrointestinal complications.4, 6, 28-31 The current study summarizes the burden attributable to chronic GvHD by demonstrating a 4-fold increased risk of severe/life-threatening health conditions among patients with active chronic GvHD. The chronic health conditions reported include those that are well known consequences of chronic GvHD and its management, ie, visual impairment, gastrointestinal complications, and musculoskeletal disabilities. It is noteworthy that the prevalence of active chronic GvHD did not differ by ethnicity in the current study.
Complications associated with TBI include renal insufficiency,30, 32 cataracts,33-35 cardiopulmonary dysfunction,29, 36-38 endocrinopathies,39-41 and subsequent malignancies.42-44 Several of these conditions, such as cataracts, chronic renal insufficiency, and pulmonary dysfunction, in turn, are exacerbated by chronic GvHD and its treatment. In the current study, individuals who received TBI reported a nearly 2-fold increased risk of severe or life-threatening chronic health conditions independent of chronic GvHD status.
The results from this study must be interpreted in the context of potential limitations. Hispanics were over represented among nonparticipants, potentially contributing to an underestimation of chronic health conditions in this population of survivors if nonparticipants had a greater prevalence of chronic health conditions than participants. However, nonparticipants were younger at the time of HCT and at the time of survey and were less likely to have received TBI—characteristics that are associated with a lower risk of chronic health conditions—suggesting that nonparticipants should have been at a lower risk of developing these complications than participants and, thus, not resulting in an underestimation of the prevalence.
Ethnic differences in mortality because of chronic health conditions before study participation potentially could have introduced bias in the prevalence of chronic health conditions reported by the survivors. However, we did not observe ethnic/racial differences in nonrecurrence-related late mortality after HCT.5, 6 Therefore, we believe that ethnic differences in mortality caused by chronic health conditions would not have contributed to bias in the current study.
This study was designed to capture self-reported chronic health conditions that were diagnosed as a consequence of the delivery of “standard care” after HCT. Large studies of cancer cohorts have demonstrated that self-report can be used effectively to describe post-treatment complications that are diagnosed as part of routine healthcare delivery.14, 39, 45-47 Furthermore, we have demonstrated that HCT survivors have the ability to report post-HCT complications accurately12 as long as they have been diagnosed, which depends on access to care, which, in turn, depends on the availability of health insurance coverage.
The current study was not designed to conduct a comprehensive evaluation of all HCT survivors that identifies preclinical or clinically overt, long-term complications—an approach that is needed to describe the burden of long-term morbidity in all patient populations but that, logistically and financially, was prohibitive in a large and geographically diverse cohort like ours. Conversely, in this report, we summarize the prevalence of chronic health conditions that are diagnosed by our healthcare system, taking into account issues related to health insurance coverage, access to care, awareness among the healthcare providers of the risk of long-term complications, and the communication of these outcomes to HCT survivors. Keeping these issues in mind, we observed that Hispanics were less likely to report severe/life-threatening health conditions after HCT—a difference that decreased in magnitude and significance after taking health insurance into consideration. Although our results confirmed the role of TBI and chronic GvHD, we identified the role of health insurance coverage as a mediator of the lower prevalence of self-reported, long-term morbidity in Hispanic HCT survivors.
CONFLICT OF INTEREST DISCLOSURES
Supported by National Institutes of Health grants R01 CA078938 (S. Bhatia) and P01 CA30206 (S. Forman) and by a Lymphoma/Leukemia Society Scholar Award for Clinical Research 2192 (S. Bhatia).
- 9Board on Health Sciences Policy. Unequal Treatment: Confronting Racial and Ethnic Disparities in Health Care. Washington, DC: National Academy Press; 2002.
- 10U.S. Census Bureau. Census 2005. American Fact Finder. Washington, DC: U.S. Census Bureau; 2005.
- 19Centers for Disease Control and Prevention. National Center for Health Statistics. Health Data Interactive, 2007. Available at: http://www.cdc.gov/nchs/hdi.htm. Accessed February 17, 2009.
- 29Impact of cumulative anthracycline dose, preparative regimen and chronic graft-versus-host disease on pulmonary and cardiac function in children 5 years after allogeneic hematopoietic stem cell transplantation: a prospective evaluation on behalf of the EBMT Pediatric Diseases and Late Effects Working Parties. Bone Marrow Transplant. 2007; 39: 667-675., , , et al.
- 33Visual, auditory, sensory, and motor impairments in long-term survivors of hematopoietic stem cell transplantation performed in childhood: results from the Bone Marrow Transplant Survivor Study. Cancer. 2006; 106: 1402-1408., , , et al.