American Journal of Epidemiology Advance Access originally published online on February 26, 2007
American Journal of Epidemiology 2007 165(11):1255-1264; doi:10.1093/aje/kwm020
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
ORIGINAL CONTRIBUTIONS |
Ultraviolet Radiation Exposure and Risk of Non-Hodgkin's Lymphoma
1 Yale University School of Epidemiology and Public Health, New Haven, CT
2 International Agency for Research on Cancer, Lyon, France
3 Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT
4 Department of Epidemiology and Biostatistics, McGill University, Montreal, Canada
5 Maine Center for Toxicology and Environmental Health, University of South Maine, Portland, ME
6 Department of Surgery, Harvard School of Public Health, Boston, MA
Correspondence to Dr. Yawei Zhang, Yale University School of Public Health, 60 College Street, LEPH 440, P.O. Box 208034, New Haven, CT 06520-8034 (e-mail: yawei.zhang{at}yale.edu).
Received for publication June 5, 2006. Accepted for publication November 17, 2006.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Sun exposure has been suggested to increase the risk of non-Hodgkin's lymphoma. The authors analyzed data from a population-based, case-control study of Connecticut women between 1996 and 2000 to study the hypothesis. Women who reported having had a suntan experienced an increased risk of non-Hodgkin's lymphoma with increasing duration (ptrend = 0.0062) compared with women who reported never having had a suntan. An almost threefold increased risk of non-Hodgkin's lymphoma was observed among women who reported having had a suntan for less than 3 months per year and a suntan history of more than 60 years (odds ratio = 2.8, 95% confidence interval: 1.6, 4.9) compared with those who reported never having had a suntan. For women who reported having spent time in strong sunlight between 9 a.m. and 3 p.m. during the summer, a 70% increased risk of non-Hodgkin's lymphoma was observed for the highest tertile of duration compared with the lowest (odds ratio = 1.7, 95% confidence interval: 1.2, 2.4). The risk increased with increasing duration of time spent in strong sunlight in summer (ptrend = 0.0051). The risk appears to vary by non-Hodgkin's lymphoma subtypes. Further investigations of the role of ultraviolet radiation on the risk of non-Hodgkin's lymphoma are warranted.
case-control studies; lymphoma, non-Hodgkin; radiation, nonionizing; ultraviolet rays
Abbreviations: CI, confidence interval; OR, odds ratio
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
The incidence of non-Hodgkin's lymphoma has been increasing worldwide during the past several decades. It is suggested that increasing exposure to ultraviolet radiation may be at least in part responsible for the observed increase in incidence of non-Hodgkin's lymphoma (1). A potential relation between ultraviolet radiation exposure and non-Hodgkin's lymphoma risk is biologically plausible since experimental studies have shown that ultraviolet radiation induces systemic immunosuppression (2), which is a well-established risk factor for non-Hodgkin's lymphoma (3).
This relation is also supported by earlier epidemiologic observations that indirectly investigated the relation between ultraviolet radiation exposure and non-Hodgkin's lymphoma risk. For example, studies showed that an increased risk of non-Hodgkin's lymphoma was associated with a previous diagnosis of skin cancer and vice versa (4, 5). Several ecologic studies also reported a positive correlation between ambient ultraviolet radiation level and non-Hodgkin's lymphoma incidence or mortality (6–8), although several others did not support the association (9–11). An epidemiologic study using geographic latitude as an indicator for sun exposure also showed a positive association between sun exposure and non-Hodgkin's lymphoma risk (12). Among three epidemiologic studies using outdoor occupation as surrogate measure for sun exposure, one (13) found an increased risk of non-Hodgkin's lymphoma associated with occupational exposure to sunlight, while the others found no such association (12, 14).
Two recent epidemiologic studies directly examined the relation between reported sun exposure history and non-Hodgkin's lymphoma risk; however, both found an inverse association between ultraviolet radiation and non-Hodgkin's lymphoma risk (15, 16). Hughes et al. (16) reported a 30 percent reduced risk of non-Hodgkin's lymphoma for people in the highest quartile of total hours spent outdoors between 9 a.m. and 5 p.m., compared with those in the lowest quartile. The association was strengthened for time spent outdoors between 9 a.m. and 5 p.m. on nonworking days. Smedby et al. (15) reported that a high frequency of sun bathing and sunburns at age 20 years and 5–10 years before the interview was associated with a 30–40 percent reduced risk of non-Hodgkin's lymphoma.
Human exposure to ultraviolet radiation has been increasing during the past several decades as a result of the social desire for tanned skin, change in clothing patterns, increasing outdoor recreational activities, or increasing amounts of ultraviolet radiation reaching the earth's surface from the depletion of the ozone layer (17). Considering the increasing exposure to ultraviolet radiation and the limited and conflicting literature on the relation between ultraviolet radiation exposure and non-Hodgkin's lymphoma risk, there exists an urgent need to understand the relation between ultraviolet radiation exposure and non-Hodgkin's lymphoma risk. Here, we reported the results linking ultraviolet radiation to non-Hodgkin's lymphoma risk from a population-based, case-control study of non-Hodgkin's lymphoma in Connecticut women.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Study population
A detailed description of the study population has been described elsewhere (18–20). Briefly, the cases included in the study were histologically confirmed, incident non-Hodgkin's lymphoma patients diagnosed in Connecticut between 1996 and 2000, who had no previous diagnosis of cancer with the exception of nonmelanoma skin cancer. A total of 832 incident female non-Hodgkin's lymphoma cases, aged 21–84 years at diagnosis, were ascertained through the Rapid Case Ascertainment Shared Resource at the Yale Cancer Center during the study period, with 601 of them (72 percent) completing in-person interviews.
Pathology slides (or tissue blocks) were obtained for non-Hodgkin's lymphoma cases from the pathology departments where the cases were diagnosed for histologic classification. Each specimen was independently reviewed by two study pathologists, who were experienced in the diagnosis of lymphoma. Non-Hodgkin's lymphoma cases were classified according to the World Health Organization's classification system.
Population-based female controls with Connecticut addresses were recruited by use of random digit dialing methods for those under the age of 65 years or randomly selected from the files provided by the Centers for Medicare and Medicaid Service for those aged 65 or more years. The participation rate was 69 percent for random digit dialing controls and 47 percent for Centers for Medicare and Medicaid Service controls. Cases and controls were frequency matched by age (±5 years).
Interviews
All procedures were performed in accordance with a protocol approved by the human investigation committees at Yale University, the Connecticut Department of Public Health, and the National Cancer Institute. A standardized, structured questionnaire was used to collect information on recreational and occupational ultraviolet radiation exposure history, as well as on other major known or suspected risk factors that might confound the association between ultraviolet radiation exposure and non-Hodgkin's lymphoma risk through an in-person interview.
Information on recreational ultraviolet radiation exposure was obtained for four age periods: less than 18 years, between 18 and 40 years, between 41 and 60 years, and more than 60 years. Subjects were first asked about their suntan history, including years of having a suntan and months per year of having a suntan. Subjects were then asked about the hours per day during the weekdays and weekends they usually spent in strong sunlight (between 9 a.m. and 3 p.m.) and the years of staying in strong sunlight during the summer time. Finally, subjects were asked whether they had spent time (lived or stayed for vacation) in the tropics when they were at each age period. If so, subjects were asked about the total weeks they stayed at these places during each age period. The history of using an artificial sunlamp was also collected, including the type of sunlamp used, the minutes of use each time, the duration in years of use, and the total times of use. For the history of occupational exposure to ultraviolet radiation, subjects were asked to provide all job titles and main duties that they had for 1 year or longer before diagnosis (for cases) or interview (for controls). Each job title was designated as indoor (purely indoor or mixed type) or outdoor. If an individual had both indoor and outdoor jobs, she was assigned to the outdoor job category.
Data analysis
An unconditional logistic regression model was used to estimate the association between exposure to ultraviolet radiation and risk of non-Hodgkin's lymphoma. Several exposure variables were created in assessing ultraviolet radiation exposure and non-Hodgkin's lymphoma risk: Lifetime duration in years of having suntan and lifetime duration in years of spending time in strong sunlight were created by summing the duration in years for all four age periods for these two events. The reported number of average months per year of having suntan was calculated by first summing the average months per year at each age period and then dividing by four (periods). The total number of hours per week of spending time in strong sunlight was calculated by first adding the total hours per week at each age period and then dividing by four (periods). Continuous variables were categorized according to the distributions among control subjects. Formal testing for linear trend was performed by assigning values of 1, 2, 3, and 4 for quartile or 1, 2, 3 for tertile exposure groups.
The identification of potential confounding variables was based on data reported in previous studies. Confounding variables that resulted in a material change in the risk estimate, either individually or as a group, were included in the final model. Age, race, family history of non-Hodgkin's lymphoma, and the highest level of education were included in the final model. A total of 295 subjects provided information on eye color and skin type, and these variables have also been included in the final model. Adjustments for other variables, such as natural hair color, smoking, and alcohol consumption, did not result in any material change of the observed associations and, thus, were not included in the final model.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
As shown in table 1, women who reported having had the longest duration of suntan experienced an increased risk of non-Hodgkin's lymphoma. Compared with women who reported never having had a suntan, those who reported having had a history of suntan for 60 years or more experienced a 50 percent increased risk of non-Hodgkin's lymphoma (odds ratio (OR) = 1.5, 95 percent confidence interval (CI): 1.0, 2.5). Analyses by years of suntan for each age period showed similar patterns except for the age period 18–40 years. Women who reported a history of suntan for 14 or more years after the age of 60 years had about twice the risk of non-Hodgkin's lymphoma (OR = 1.9, 95 percent CI: 1.2, 3.1) compared with those who reported that they never had suntan after age 60 years. The risk of non-Hodgkin's lymphoma increased with increasing duration (ptrend = 0.0040). An increased risk of non-Hodgkin's lymphoma associated with suntan was seen mainly among women who reported an irregular (or shorter) duration of suntan per year.
|
Women who reported having spent time in strong sunlight (between 9 a.m. and 3 p.m.) during the summer experienced an increased risk of non-Hodgkin's lymphoma (table 1). A 70 percent (95 percent CI: 1.2, 2.4) increased risk was observed for those who reported having had the longest lifetime duration of spending time in strong sunlight during summer. Analyses by age periods showed a similar risk pattern associated with time spent in strong sunlight, except for the age period 18–40 years. No clear risk pattern was observed for the hours per week spent in strong sunlight. Women who reported having spent time in the tropics did not show a clear increased risk of non-Hodgkin's lymphoma either. The reported history of having two or more sunburns was associated with a slightly reduced risk of non-Hodgkin's lymphoma, although none of the odds ratios was statistically significant.
The risk of non-Hodgkin's lymphoma associated with sun exposure by age at diagnosis is presented in table 2. Although no increased risk was associated with history of suntan for women who were aged less than 65 years, a 70–80 percent increased risk of non-Hodgkin's lymphoma was associated with history of suntan for women who were aged 65 years or more at diagnosis. An increased risk of non-Hodgkin's lymphoma was associated with duration (number of years) spent in strong sunlight during the summer in both age groups. However, the number of hours per week spent in strong sunlight during the summer was associated with an increased risk of non-Hodgkin's lymphoma only among women who were aged 65 years or more.
|
The results linking duration (number of years) of having a suntan to non-Hodgkin's lymphoma risk, according to months per year (<3 months per year and
3 months per year), are presented in table 3. The increased risk of non-Hodgkin's lymphoma associated with increasing duration (number of years) of having a suntan was observed only among women who reported having had a suntan for less than 3 months per year (ptrend < 0.0001). Women who reported having had a suntan for 60 years or more experienced about a threefold increased risk of non-Hodgkin's lymphoma compared with those who never had a suntan (OR = 2.8, 95 percent CI: 1.6, 4.9). This study, however, found no increased risk of non-Hodgkin's lymphoma for those who reported having had a suntan for 3 or more months per year. The risk associated with history of suntan was seen mainly in women who were aged 65 years or more.
|
The results linking sunlight exposure to non-Hodgkin's lymphoma risk by non-Hodgkin's lymphoma subtype are presented in table 4. Although stratification by non-Hodgkin's lymphoma subtype made the estimate less stable, a generally increased risk of non-Hodgkin's lymphoma associated with longer duration of having a suntan (in years) and duration of time spent in strong sunlight during summer was observed for B-cell lymphoma (ptrend = 0.033 and 0.019, respectively), particularly for chronic lymphocytic leukemia/small lymphocytic lymphoma (ptrend = 0.0077 and 0.0060, respectively). Women who reported having vacationed in the tropics experienced a 60 percent increased risk of diffuse large B-cell lymphoma (OR = 1.6, 95 percent CI: 1.1, 2.3). On the other hand, the reported history of sunburn was generally negatively associated with non-Hodgkin's lymphoma subtype.
|
The results linking sunlamp use and occupational sun exposure to non-Hodgkin's lymphoma risk are presented in table 5. Sunlamp use was not significantly associated with the risk of non-Hodgkin's lymphoma by duration, by overall intensity, or by subtype. Outdoor occupation was associated with an 80 percent increased risk of non-Hodgkin's lymphoma (95 percent CI: 1.0, 3.4).
|
We also analyzed the data for non-Hispanic Caucasians only and have reached the same conclusions as presented for the overall population (the results are available upon request).
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
The results from this study suggest that long-term, irregular sun exposure may be associated with an increased risk of non-Hodgkin's lymphoma and that the increased risk may vary by non-Hodgkin's lymphoma subtype. Our study found that an increased risk of non-Hodgkin's lymphoma was seen mainly among women who had a history of having suntans or spending time in strong sunlight for the highest tertile of duration, indicating that long-term exposure to strong sunlight may be necessary for ultraviolet radiation to play a role in lymphogenesis. Our results from linear trend tests showed that the risk of non-Hodgkin's lymphoma increased with increasing duration of reported years of having suntans or years of spending time in strong sunlight during the summer.
On the basis of the experience from the study of sun exposure and malignant melanoma in Connecticut (21), we asked study subjects whether they had a suntan for less than 3 months or 3 or more months per year. Those who reported having had a suntan for less than 3 months per year were considered to have had irregular sun exposure. In our study, stratification by months per year of having a suntan showed that an increased risk of non-Hodgkin's lymphoma was seen only among women who reported having had a suntan for less than 3 months per year, while no increased risk was observed for women who reported having had a suntan for 3 or more months per year. Tanning of the skin is caused by an increase in the release of the pigment melanin into the skin's cells after exposure to ultraviolet radiation, which protects the body from absorbing an excess of ultraviolet radiation. It is possible that prolonged exposure to sunlight from regular suntan may have helped to develop pigmentation, which would help to reduce the absorption of ultraviolet radiation. Studies of sun exposure and melanoma have shown that intermittent sun exposure plays a more important role in the pathogenesis of melanoma (22). It is suggested that the intermittent stimulation of ultraviolet radiation has a more powerful promotional effect than does continuous stimulation in the development of melanoma (23). On the other hand, the duration of suntans for an individual in a given year can be affected by many factors, such as the ability to have suntan. Some people easily get sunburns, while others can enjoy a constant suntan. The negative correlation between skin sensitivity to sunlight and months per year of having a suntan (Pearson's correlation coefficient = –0.34, p < 0.0001) in our study suggests that people who are sensitive to sunlight are likely to reduce their exposure to sunlight. Thus, it is likely that, by trying to avoid constant sun exposure and suntans/sunburns, people who are sensitive to sunlight will report a shorter duration of sun exposure in a given year. In addition, the avoidance of constant sun exposure would lead to irregular sun exposure and result in a shorter duration of suntan in a given year.
Two recent epidemiologic studies (15, 16) with individual ultraviolet radiation exposure information, however, reported a reduced risk of non-Hodgkin's lymphoma associated with ultraviolet radiation. Hughes et al. (16) from Australia reported that risk of non-Hodgkin's lymphoma decreased with increasing reported sun exposure hours (ptrend = 0.01). Specifically, those in the highest quartile of total hours spent outdoors between 9 a.m. and 5 p.m. had a 35 percent reduced risk of non-Hodgkin's lymphoma (OR = 0.65, 95 percent CI: 0.46, 0.91) compared with those in the lowest quartile. The inverse association was further strengthened for time spent outdoors during nonworking days (ptrend = 0.0001). Additionally, they found a nonsignificantly increased risk of non-Hodgkin's lymphoma for lifetime occupational sun exposure when they compared those in the highest exposure tertile (OR = 1.21, 95 percent CI: 0.87, 1.69) with those never exposed to occupational sunlight.
Smedby et al. (15) from Sweden reported that those with a high frequency of sunbathing and sunburns at age 20 years and 5–10 years before the interview had a 30–40 percent reduced risk of non-Hodgkin's lymphoma compared with those who never sunbathed or had sunburns at age 20 years and 5–10 years before the interview. They found a 10–20 percent increased risk among those who ever had outdoor occupations, which is consistent with the findings from the study by Hughes et al. (16). Our study found an 80 percent (95 percent CI: 1.0, 3.4) increased risk of non-Hodgkin's lymphoma associated with outdoor occupation.
It is difficult to directly compare the study results reported by Smedby et al. (15), Hughes et al. (16), and the current study. These three studies have used very different definitions of exposure to ultraviolet radiation in their assessments. In the study by Smedby et al. (15), sunbathing was used as the index for ultraviolet radiation exposure, and information was collected on sunbathing frequency at the age of 20 years and at 5–10 years before the interview. In the study by Hughes et al. (16), the time spent outdoors was used to measure sun exposure. Information was collected on the total hours spent outdoors between 9 a.m. and 5 p.m. on working or school days, nonworking days or weekends, and vacations in the warmer and cooler months for the years the subjects turned 10, 20, 30, 40, 50, and 60 years of age. In our study, subjects were asked about their suntan history, including the number of years having a suntan and months per year of having a suntan; hours per day spent in strong sunlight (between 9 a.m. and 3 p.m.) during weekdays and weekends; and the number of years of staying in strong sunlight during the summer time for four age periods: <18, 18–40, 41–60, and >60 years. Use of different definitions of sun exposure, in addition to the collection of sun exposure data during different lifetime periods, would have contributed to some of the inconsistent results reported in the various studies. Use of different disease definitions in the three studies may have also contributed to the inconsistent results observed in these studies.
In order to have a better comparison of our study with the study by Smedby et al. (15), we did an analysis for the last age period of exposure to ultraviolet radiation for a period comparable to that in the study by Smedby et al. (15), 5–10 years before the interview. We found an increased risk for women who reported having had a history of suntan for less than 3 months per year (OR = 1.6, 95 percent CI: 1.2, 2.2) and for women in the tertile who reported the most hours per week of time spent in strong sunlight during the summer (OR = 1.3, 95 percent CI: 0.9, 1.7).
The relation between ultraviolet radiation and non-Hodgkin's lymphoma risk is biologically plausible. Ultraviolet radiation has been shown to cause immunosuppression, and immunosuppression is a well-established risk factor for non-Hodgkin's lymphoma. Fisher and Kripke (24) reported that ultraviolet-irradiated mice failed to reject highly antigenic tumor cells. It has been shown that ultraviolet radiation induces expression of interleukin 10 and tumor necrosis factor 
(25, 26). Knockout mice show that both cytokines play a critical role in B-cell lymphogenesis (27). An elevated serum level of interleukin 10 has been found in a variety of B-cell malignancies (28). A recent report from the InterLymph Consortium by Rothman et al. (29) showed that genetic variations in tumor necrosis factor and interleukin 10 were associated with an increased risk of non-Hodgkin's lymphoma. In addition to interleukin 10 and tumor necrosis factor , ultraviolet radiation induces interleukin 6, which has been suggested as a potent growth factor for intermediate- and high-grade B-cell lymphomas (30).
Ultraviolet radiation induces DNA damage by forming DNA photoproducts, which are removed mainly by nucleotide excision repair (31). Thus, genetic susceptibility may also affect the responses to sun exposure by different populations. Although no study, so far, has examined the potential gene-environmental interactions between sun exposure and genetic polymorphisms on non-Hodgkin's lymphoma risk, studies of skin cancer have shown that genetic polymorphisms of the xeroderma pigmentosum group D (XPD) gene, a gene involved in the nucleotide excision repair pathway removing DNA photoproducts, modify the relation between sun exposure and skin cancer risk (32). Future studies are needed to investigate the potential interaction between sun exposure and genetic polymorphisms on the risk of non-Hodgkin's lymphoma.
It should be noted that, in this study, we found that the reported history of sunburns was not positively associated with the risk of non-Hodgkin's lymphoma. The lack of a positive association between reported history of sunburn and non-Hodgkin's lymphoma risk could be explained by the fact that there was a negative correlation between reported history of sunburns and lifetime duration of suntans (Pearson's correlation coefficient = –0.065, p = 0.018). The negative correlation suggests that sunburn history reflects an individual's ability to have suntan and has a direct impact on history of sun exposure and prevention behaviors. As such, the observed association between reported history of sunburns and reduced risk of non-Hodgkin's lymphoma actually reflects the effect from a reduced sun exposure.
Sunlamp use was not associated with an increased risk of non-Hodgkin's lymphoma in the current study either. More than 75 percent of the sunlamp users in our study reported having used sunlamps for less than 5 years, and less than 5 percent of subjects reported having used sunlamps for 20–40 years. The lack of association between sunlamp use and non-Hodgkin's lymphoma risk observed in this study may suggest that long-term exposure to ultraviolet radiation may be needed for ultraviolet radiation to play a role in lymphogenesis.
In this study, the information on individual lifetime sun exposure was collected from in-person interviews, where some misclassification of sun exposure through subjects' recall was unavoidable, particularly for early life exposures. However, misclassification was unlikely differential between cases and controls. Selection bias is always a concern in epidemiologic studies when a substantial number of eligible subjects refuse to participate. However, refusal to participate must be associated with both the exposure and the disease of interest in order to introduce selection bias. Because the interviewees were not informed of the study hypothesis, and because the general population had little knowledge of the potential relation between sun exposure and non-Hodgkin's lymphoma at the time when the study was conducted, selection bias resulting from the refusal to participate appears to be an unlikely explanation for the observed association. On the other hand, it is possible that healthier controls are more likely to participate in research and are therefore more likely to spend time in the sun, whereas unhealthy people are more likely to spend less time in the sun. If this is indeed the case, selection of healthier controls in our study could result in an underestimation of the association between ultraviolet radiation exposure and non-Hodgkin's lymphoma risk.
Exclusion of subjects with a previous diagnosis of malignant melanoma may have led to the exclusion of subjects that are more susceptible to sun exposure, thus resulting in a potential underestimation of the observed association between non-Hodgkin's lymphoma and sun exposure. In this study, information on skin type and eye color was collected from 22 percent of the participants. Previous studies showed that adjustment for skin type and eye color did not result in material changes to their observed association between sun exposure and non-Hodgkin's lymphoma risk (15, 16). Thus, it is unlikely that the observed association in our study is severely confounded by incomplete information of eye color and skin type. We did not collect detailed information on sun-shielding clothing and hats worn during outdoor occupational and recreational sun exposure, which limited our ability to analyze ultraviolet radiation exposure and non-Hodgkin's lymphoma risk by these variables. However, while the lack of information on clothing and hats may have introduced exposure misclassification, the exposure misclassification would probably be nondifferential, resulting in an underestimation of the association between sun exposure and non-Hodgkin's lymphoma risk. It should also be noted that, although we had a relatively large sample size, the study power for the subtype analyses may still be limited. Given the number of comparisons carried out in this study, chance alone cannot be entirely ruled out as a potential explanation for the observed associations in this study. Additionally, as our study included only women, caution must be exercised when making inferences to men.
In summary, this population-based, case-control study found that women who reported having spent more than 40 years in strong sunlight during summer had a 30–70 percent increased risk of non-Hodgkin's lymphoma. Women who reported having had a suntan for less than 3 months per year for more than 60 years experienced about a threefold increased risk of non-Hodgkin's lymphoma. Additionally, the increased risk of non-Hodgkin's lymphoma associated with sun exposure appears to vary by non-Hodgkin's lymphoma subtypes. Further studies are warranted to investigate whether genetic susceptibility may modify the relation between sun exposure and risk of non-Hodgkin's lymphoma.
|
ACKNOWLEDGMENTS |
|---|
This study is supported by grant CA62006 from the National Cancer Institute. Certain data used in this study were obtained from the Connecticut Tumor Registry located in the Connecticut Department of Public Health.
The authors thank the institutions that allowed access to diagnostic materials and pathology reports, including the following hospitals: Charlotte Hungerford Hospital, Danbury Hospital, Greenwich Hospital, Griffin Hospital, Hartford Hospital, Johnson Memorial Hospital, Middlesex Hospital, Lawrence and Memorial Hospital, New Britain General Hospital, Bradley Memorial Hospital, Norwalk Hospital, St. Francis Hospital and Medical Center, St. Mary's Hospital, Hospital of St. Raphael, St. Vincent's Medical Center, Stamford Hospital, William W. Backus Hospital, Waterbury Hospital, Yale-New Haven Hospital, Manchester Memorial Hospital, Rockville General Hospital, Bridgeport Hospital, Windham Hospital, Sharon Hospital, Milford Hospital, New Milford Hospital, Bristol Hospital, MidState Medical Center, and Day-Kimball Hospital.
The authors assume full responsibility for analyses and interpretation of these data.
Conflict of interest: none declared.
|
References |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
- Zheng T, Mayne ST, Boyle P, et al. Epidemiology of non-Hodgkin lymphoma in Connecticut. 1935 –1988. Cancer (1992) 70:840–9.[CrossRef][Web of Science][Medline]
- Kripke ML. Effects of UV radiation on tumor immunity. J Natl Cancer Inst (1990) 82:1392–6.
[Free Full Text] - Hoover RN. Lymphoma risks in populations with altered immunity—a search for mechanism. Cancer Res (1992) 52(suppl):5477s–8s.
[Abstract/Free Full Text] - Levi F, Randimbison L, Te VC, et al. Non-Hodgkin's lymphomas, chronic lymphocytic leukaemias and skin cancers. Br J Cancer (1996) 74:1847–50.[Web of Science][Medline]
- Adami J, Frisch M, Yuen J, et al. Evidence of an association between non-Hodgkin's lymphoma and skin cancer. BMJ (1995) 310:1491–5.
[Abstract/Free Full Text] - McMichael AJ, Giles GG. Have increases in solar ultraviolet exposure contributed to the rise in incidence of non-Hodgkin's lymphoma? Br J Cancer (1996) 73:945–50.[Web of Science][Medline]
- Langford IH, Bentham G, McDonald AL. Mortality from non-Hodgkin lymphoma and UV exposure in the European Community. Health Place (1998) 4:355–64.[CrossRef][Medline]
- Bentham G. Association between incidence of non-Hodgkin's lymphoma and solar ultraviolet radiation in England and Wales. BMJ (1996) 312:1128–31.
[Abstract/Free Full Text] - Hartge P, Devesa SS, Grauman D, et al. Non-Hodgkin's lymphoma and sunlight. J Natl Cancer Inst (1996) 88:298–300.
[Free Full Text] - Hu S, Ma F, Collado-Mesa F, et al. Ultraviolet radiation and incidence of non-Hodgkin's lymphoma among Hispanics in the United States. Cancer Epidemiol Biomarkers Prev (2004) 13:59–64.
[Abstract/Free Full Text] - Newton R. Solar ultraviolet radiation is not a major cause of primary cutaneous non-Hodgkin's lymphoma. BMJ (1997) 314:1483–4.
[Free Full Text] - Adami J, Gridley G, Nyren O, et al. Sunlight and non-Hodgkin's lymphoma: a population-based cohort study in Sweden. Int J Cancer (1999) 80:641–5.[CrossRef][Web of Science][Medline]
- Hakansson N, Floderus B, Gustavsson P, et al. Occupational sunlight exposure and cancer incidence among Swedish construction workers. Epidemiology (2001) 12:552–7.[CrossRef][Web of Science][Medline]
- van Wijngaarden E, Savitz DA. Occupational sunlight exposure and mortality from non-Hodgkin lymphoma among electric utility workers. J Occup Environ Med (2001) 43:548–53.[CrossRef][Web of Science][Medline]
- Smedby KE, Hjalgrim H, Melbye M, et al. Ultraviolet radiation exposure and risk of malignant lymphomas. J Natl Cancer Inst (2005) 97:199–209.
[Abstract/Free Full Text] - Hughes AM, Armstrong BK, Vajdic CM, et al. Sun exposure may protect against non-Hodgkin lymphoma: a case-control study. Int J Cancer (2004) 112:865–71.[CrossRef][Web of Science][Medline]
- Norval M. Effects of solar radiation on the human immune system. J Photochem Photobiol B (2001) 63:28–40.[CrossRef][Medline]
- Zhang Y, Holford TR, Leaderer B, et al. Blood transfusion and risk of non-Hodgkin's lymphoma in Connecticut women. Am J Epidemiol (2004) 160:325–30.
[Abstract/Free Full Text] - Zhang Y, Holford TR, Leaderer B, et al. Menstrual and reproductive factors and risk of non-Hodgkin's lymphoma among Connecticut women. Am J Epidemiol (2004) 160:766–73.
[Abstract/Free Full Text] - Zhang Y, Holford TR, Leaderer B, et al. Prior medical conditions and medication use and risk of non-Hodgkin lymphoma in Connecticut United States women. Cancer Causes Control (2004) 15:419–28.[CrossRef][Web of Science][Medline]
- Chen YT, Dubrow R, Zheng T, et al. Sunlamp use and the risk of cutaneous malignant melanoma: a population-based case-control study in Connecticut, USA. Int J Epidemiol (1998) 27:758–65.
[Abstract/Free Full Text] - Elwood JM. Melanoma and sun exposure: contrasts between intermittent and chronic exposure. World J Surg (1992) 16:157–65.[CrossRef][Web of Science][Medline]
- Holman CD, Armstrong BK, Heenan PJ. A theory of the etiology and pathogenesis of human cutaneous malignant melanoma. J Natl Cancer Inst (1983) 71:651–6.[Web of Science][Medline]
- Fisher MS, Kripke ML. Systemic alteration induced in mice by ultraviolet light irradiation and its relation to ultraviolet carcinogenesis. 1977. Bull World Health Organ (2002) 80:908–12.[Web of Science][Medline]
- Nishigori C, Yarosh DB, Ullrich SE, et al. Evidence that DNA damage triggers interleukin 10 cytokine production in UV-irradiated murine keratinocytes. Proc Natl Acad Sci U S A (1996) 93:10354–9.
[Abstract/Free Full Text] - Kibitel J, Hejmadi V, Alas L, et al. UV-DNA damage in mouse and human cells induces the expression of tumor necrosis factor alpha. Photochem Photobiol (1998) 67:541–6.[CrossRef][Web of Science][Medline]
- Czarneski J, Lin YC, Chong S, et al. Studies in NZB IL-10 knockout mice of the requirement of IL-10 for progression of B-cell lymphoma. Leukemia (2004) 18:597–606.[CrossRef][Web of Science][Medline]
- Aydin F, Yilmaz M, Ozdemir F, et al. Correlation of serum IL-2, IL-6 and IL-10 levels with International Prognostic Index in patients with aggressive non-Hodgkin's lymphoma. Am J Clin Oncol (2002) 25:570–2.[CrossRef][Web of Science][Medline]
- Rothman N, Skibola CF, Wang SS, et al. Genetic variation in TNF and IL10 and risk of non-Hodgkin lymphoma: a report from the InterLymph Consortium. Lancet Oncol (2006) 7:27–38.[CrossRef][Web of Science][Medline]
- Emilie D, Coumbaras J, Raphael M, et al. Interleukin-6 production in high-grade B lymphomas: correlation with the presence of malignant immunoblasts in acquired immunodeficiency syndrome and in human immunodeficiency virus-seronegative patients. Blood (1992) 80:498–504.
[Abstract/Free Full Text] - Wood RD. Nucleotide excision repair in mammalian cells. J Biol Chem (1997) 272:23465–8.
[Free Full Text] - Han J, Colditz GA, Liu JS, et al. Genetic variation in XPD, sun exposure, and risk of skin cancer. Cancer Epidemiol Biomarkers Prev (2005) 14:1539–44.
[Abstract/Free Full Text]
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||