This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Clarke, C. A. Articles by Holly, E. A. Search for Related Content PubMed PubMed Citation Articles by Clarke, C. A. Articles by Holly, E. A.

Changes in Cancer Registry Coding for Lymphoma Subtypes: Reliability Over Time and Relevance for Surveillance and Study

¹ Northern California Cancer Center, Fremont, California; ² National Cancer Institute, NIH/Department of Health and Human Services, Rockville, Maryland; and ³ University of California San Francisco, San Francisco, California

Requests for reprints: Christina Clarke, Northern California Cancer Center, 2201 Walnut Avenue #300, Fremont, CA 94538. Phone: 510-608-5000; Fax: 510-608-5085. E-mail: tina{at}nccc.org

	Abstract

Top Abstract Introduction Materials and Methods Results Discussion References

 
Because lymphoma comprises numerous histologic subtypes, understanding the reasons for ongoing increases in its incidence requires surveillance and etiologic study of these subtypes. However, this research has been hindered by many coexisting classification schemes. The Revised European American classification of Lymphoid Neoplasms (REAL)/WHO system developed in 1994 and now used in clinical settings was not incorporated into the International Classification of Diseases-Oncology (ICD-O), used by cancer registries, until the release of the third edition (ICD-O-3) in 2001. Studies including patients diagnosed before 2001 may have codes from earlier ICD-O versions that must be converted to ICD-O-3 and have higher proportions of unclassified (e.g., lymphoma and not otherwise specified) cases. To better understand (a) the agreement of computer-converted ICD-O-3 codes to ICD-O-3 codes generated directly from diagnostic pathology reports and (b) the reproducibility of unclassified status, we reviewed a population-based series of diagnostic pathology reports for lymphoma patients diagnosed before (1988-1994; n = 1,493) and after (1998-2000; n = 1,527) the REAL/WHO scheme was introduced. Overall, computer- and coder-assigned ICD-O-3 codes agreed for 77% of patients in both groups and improved slightly (82%) when codes were grouped. The most common lymphoma subtypes, diffuse large B cell and follicular, had relatively good reliability (84-89%) throughout the study period. T-cell and natural killer cell lymphomas had worse agreement than B-cell lymphomas, even when grouped. Many (42-43%) lymphomas reported as unclassifiable could be assigned a subtype upon pathology report review. These findings suggest that the study of lymphoma subtypes could be improved by (a) use of more standardized terminology in pathology reports, (b) grouping individual ICD-O-3 codes to reduce misclassification bias, and (c) routine secondary editing of unclassified lymphomas by central cancer registries. (Cancer Epidemiol Biomarkers Prev 2006;15(4):630–8)

	Introduction

Top Abstract Introduction Materials and Methods Results Discussion References

 
Lymphomas represent a large group of distinct B- and T-cell neoplasms arising from the lymphoid tissue. Overall lymphoma incidence has increased substantially in prior decades, with a 63% increase reported between 1973 and 2002 (1). Given the heterogeneity of lymphoma, understanding the reasons for this troubling increase will require the characterization and detailed etiologic study of distinct subtypes, a goal that has been hindered by the coexistence over the past three decades of multiple schemes for lymphoma classification. Although clinic-based studies used schemes like the Kiel, Lukes-Collins, Working Formulation, and the Revised European American classification of Lymphoid Neoplasms (REAL; ref. 2), which was later expanded and renamed the WHO classification, population-based studies and cancer registries used three different editions of the International Classification of Diseases-Oncology (ICD-O). The first (ICD-O-1) and second (ICD-O-2) editions (3) incorporated the Working Formulation and other now-obsolete schemes to classify lymphomas, whereas the most current third edition (ICD-O-3; ref. 4) draws heavily from the REAL/WHO scheme. ICD-O-3 has been used by cancer registries to classify cases diagnosed since the year 2001, but for cases diagnosed before 2001 and classified according to earlier versions of ICD-O, a computer algorithm has been devised to convert codes to ICD-O-3 (5).

The WHO classification represents an international consensus scheme (6) and is substantially more reliable and reproducible than prior schemes (7). Thus, the use of WHO and ICD-O-3 will simplify future monitoring and epidemiologic study of lymphoma subtypes. However, studies using historical data, such as assessments of time trends in cancer registry data, remain complicated by two issues. First, it is uncertain how well computer-generated ICD-O-3 codes agree with those directly assigned based on the original diagnostic pathology report. Of particular interest are diagnoses between 1995 and 2000 originally described by pathologists using WHO designations but coded by cancer registries to ICD-O-2. Second, cancer registry cases that are not subtyped [i.e., classified only as lymphoma and not otherwise specified (NOS)] complicate interpretation of distributions and trends of cases that are subtyped. NOS status (ICD-O-3 histology codes 9590-9591) was reported for 19% of all lymphomas reported to the National Cancer Institute's Surveillance, Epidemiology, and End Results (SEER) program between 1973 and 2002 (1). To inform the implications of these issues for future research, we obtained and reviewed a population-based series of original diagnostic pathology reports for a selection of lymphoma patients diagnosed between the years 1988 and 2000, before and after the clinical dissemination of the REAL/WHO scheme, to (a) compare the agreement of computer-assigned ICD-O-3 to that assigned from the original diagnostic text and (b) determine the reproducibility of and reasons for assigning NOS status.

	Materials and Methods

Top Abstract Introduction Materials and Methods Results Discussion References

 
Included in this study were two distinct population-based groups of lymphoma patients reported to the Greater Bay Area Cancer Registry, a participant in the (SEER) program. The first group, hereafter referred to as the "1988 to 1994 study group," included non-Hodgkin lymphoma (NHL) patients who participated in a population-based case-control study described in detail elsewhere (8-20). Patients initially eligible for the NHL study were ages 21 to 74 years and living in one of six San Francisco Bay Area counties (Alameda, Contra Costa, Marin, Santa Clara, San Francisco, or San Mateo) when newly diagnosed with NHL (ICD-O-2 morphology codes 9590-9595 and 9670-9711) from 1988 to 1994 and were identified through rapid case ascertainment procedures by the Greater Bay Area Cancer Registry. Pathology reports were collected as part of initial case ascertainment, but they were not obtained for 1,047 patients who at the time of interview were deceased or declined to participate (21). As detailed elsewhere (14), nonparticipating patients were more likely than participating patients to have more rapidly fatal lymphoma types. Of the participating patients, 61 had missing or incomplete (e.g., pages missing) pathology reports and were excluded from this analysis. Thus, the 1988 to 1994 study group included 1,493 lymphoma patients.

Patients eligible for the second group, hereafter called the "1998 to 2000 study group," included 3,673 persons of all ages living in the six aforementioned counties when diagnosed with lymphoma (ICD-O-2 histology codes 9590-9719) during the years 1998 to 2000. We sampled patients on the basis of ICD-O-2 histology code, including 100% samples of those with codes (9590, 9591, 9593, 9595, 9650, 9653-9655, 9657-9659, 9671-9675, 9677, 9680-9686, 9688, 9690, 9692, 9705, 9708-9713, and 9715-9719) that represented new or updated entities in ICD-O-3 and smaller (n = 50) random samples of those with codes (9652, 9663-9667, 9670, 9691, 9693, 9695-98, 9700-9701, 9702-9704, 9606, 9607, and 9714) that represented nearly identical entities to those described in ICD-O-3, and thereby for whom conversion was code to code or otherwise considered straightforward. Sampling yielded a total of 2,834 patients. From this group, we excluded 196 patients for whom registry data suggested that the pathology report was unavailable (i.e., due to case ascertainment from death certificate/autopsy or lack of histologic confirmation) and requested the remaining 2,638 diagnostic pathology reports. We were able to retrieve successfully 1,693 (64%) reports. Of these, 166 were deemed during review to be incomplete or otherwise inadequate, resulting in a final 1998 to 2000 study group of 1,527 lymphoma patients for whom pathology reports were successfully reviewed. These patients differed somewhat from those for whom pathology reports could not be obtained or successfully reviewed. In particular, included patients were significantly (P < 0.05) more likely to have been diagnosed in 2000 (37% versus 31%), to be residents of Contra Costa (22% versus 10%) or San Francisco counties (21% versus 16%), to have a diffuse large B-cell lymphoma (DLBCL; 49% versus 42%), and to have evidence of AIDS (10% versus 8%), but were comparable with respect to age, sex, vital status, cause of death, and diagnosis at a teaching hospital.

ICD-O-3 Code Assignment
From the Greater Bay Area Cancer Registry records, we obtained demographic information, tumor characteristics (including original ICD-O-2 histology code and the computer-converted ICD-O-3 histology code), and patient vital status as of December 31, 2003 for all study subjects. Patients were considered to have evidence of AIDS based on cancer registry AIDS-positive status or HIV-related cause of death (21). Reviewers trained by Greater Bay Area Cancer Registry–certified tumor registrars abstracted diagnostic pathology reports for information regarding type of biopsy done (surgical, core needle, fine-needle aspiration, bone marrow, peripheral blood/other), type of diagnostic specimen (fresh/frozen tissue, preserved tissue, cells from fine-needle aspiration, or tissue from fine-needle aspiration), mention of malignant cell type [B, T, natural killer (NK), other], mention of diagnostic studies done [immunohistochemistry, flow cytometry, PCR-based methods, cytogenetic studies (e.g., fluorescent in situ hybridization assays for EBV)], and whether or not the diagnosis was a referral from another physician. Finally, ICD-O-3 histology code was assigned directly from the original diagnostic text using standard ICD-O-3 documentation and guidelines and without knowledge of the original ICD-O-2 code.

For cases that were coded as NOS (ICD-O-3 histology codes 9590-9591), reviewers were asked to classify the reason why a more specific code could not be assigned (i.e., diagnostic studies not done due to poor tissue quality/sufficiency, studies not done for other reasons, studies done but not interpretable, or disease considered truly unclassifiable). Quality control measures included consultation with certified tumor registrars or a consulting pathologist when needed and reabstraction and recoding of initial reviews for 2% of patients selected randomly.

Statistical Analysis
Cross-tabulations were used for all comparisons. Agreement was quantified using the percentage of all registry diagnoses confirmed by the coder to measure the positive predictive value (22). Kappa statistics could not be used because the two rating schemes (registry and coder) did not have identical categories due to uncommon ICD-O-3 codes assigned by one but not both of the raters. ² tests were used to describe univariate differences and compare them statistically. Logistic regression was used to examine associations with multiple variables. All calculations were done using SAS version 9. For some analyses, we grouped ICD-O-3 morphology codes together into broader categories, including Burkitt lymphoma (9687 and 9826), DLBCL (9678-9680 and 9684), marginal zone lymphoma (9689 and 9699), follicular lymphoma (9690, 9691, 9695, and 9698), lymphoplasmacytic lymphoma (9671 and 9761), mantle cell lymphoma (9673), small lymphocytic lymphoma/chronic lymphocytic leukemia (9670 and 9823), mycosis fungoides/Sezary disease (9700-9701), peripheral T-cell (9702, 9705, 9708, 9714, 9716, and 9827), NK/other T-cell (9709, 9717-9719, 9831, and 9948), lymphoblastic (9727-9729 and 9835-9837) and lymphoma, NOS (9590-9591, 9596, 9675, 9820, and 9970).

	Results

Top Abstract Introduction Materials and Methods Results Discussion References

 
We reviewed 1,493 and 1,527 pathology reports from the 1988 to 1994 and 1998 to 2000 study groups, respectively. Table 1 describes demographic and other characteristics of patients comprising each study group. Patients in the 1998 to 2000 group were more likely than patients in the 1988 to 1994 group to be older, female, and non-White but were less likely to be deceased or to have evidence of AIDS, reflecting in some part the different selection criteria for the two groups. With respect to diagnostic characteristics, the 1988 to 1994 group was mostly diagnosed with a surgical biopsy (88%), with nearly half (45%) having some kind of immunohistochemical assay, but low proportions having flow cytometry (2%), assays for EBV (2%), cytogenetic studies (>1%), or molecular diagnostics (>1%). For the 1998 to 2000 group, a lower proportion (68%) was diagnosed with a surgical biopsy but had higher proportions having had immunohistochemical tests (77%), flow cytometry (13%), assays for EBV (3%), cytogenetic studies (1%), or molecular diagnostics (1%).

Agreement generally improved when codes were grouped together into a pathologist-approved grouping scheme. Tables 4 and 5 show that overall, computer-and coder-assigned subtypes agreed for 1,219 of the 1,493 patients (82%) comprising the 1988 to 1994 study group and for 1,250 of the 1,527 (82%) patients in the 1998 to 2000 group. Agreement was similar between study groups for DLBCL (at 90% and 88%) and for follicular lymphoma (at 89% and 84%). Agreement seemed to improve substantially across time periods for the mantle cell lymphoma grouping, which increased from 52% to 81%, and for the peripheral T-cell lymphoma grouping, which increased from 36% to 81%.

Lymphoma, NOS
Originally recorded by the cancer registry as lymphoma, NOS (ICD-O-3 codes 9590-9595) were 16% of the 1988 to 1994 study group and 14% of the 1998 to 2000 study group. After coder review, 14% and 13% of these groups, respectively, were so classified, including 57% of the 1988 to 1994 cases and 58% of the 1998 to 2000 cases that were originally classified as NOS. Compared with patients assigned a specific subtype, patients originally unclassified in the cancer registry were significantly (P < 0.01) more likely to have evidence of AIDS, to be deceased, male, older, and to have lived in San Francisco county. In a multivariate regression including these factors, those that were significantly and independently associated with unclassified status included evidence of AIDS (odds ratio, 2.8; 95% confidence interval, 2.0-3.9), residence in San Francisco county (odds ratio, 1.5; 95% confidence interval, 1.1-2.1), and age at diagnosis (odds ratio per year of age above 40, 1.01; 95% confidence interval, 1.00-1.02). Table 6 shows the distributions of detailed subtype assigned on re-review for 99 patients in the 1988 to 1994 study group and 80 patients in the 1998 to 2000 group that were originally unclassified. These distributions differed from those in the larger lymphoma patient population, with lower proportions of DLBCL. When compared with patients assigned a more detailed subtype upon review, the patients who remained unclassified after review (133 patients from the 1988-1994 group and 126 patients from the 1998-2000 group) did not differ by age, sex, race, diagnosis year, vital status, cause of death, and diagnosis at a teaching hospital but were significantly (P < 0.05) more likely to have evidence of AIDS (33% versus 22%) and be residents of San Francisco county (41% versus 28%). However, in multivariate regression, evidence of AIDS was the only independent predictor of remaining unclassified (odds ratio, 2.0; 95% confidence interval, 1.3-2.6). Sixty-six patients in the 1988 to 1994 study group (4% of total) and 74 patients in the 1998 to 2000 group (5% of total) were originally assigned a specific subtype but were assigned NOS status by the coder. These patients did not differ significantly with respect to demographic or hospital characteristics from patients assigned a specific code by both the registry and the coder but were more likely to have cancer registry subtype codes with mediocre or poor agreement, as described above.

	Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

Our findings also suggest that a substantial proportion (42-43%) of lymphomas initially reported to the cancer registry as NOS or unclassifiable in fact could be classified as a more detailed subtype after re-review of the diagnostic pathology report. We also observed that a small proportion of cases originally reported as a specific code were assigned NOS by the coder, but that the total proportion of cases assigned as NOS was only slightly lower for the coder-reviewed versus registry-assigned groups. Of those cases that remained unclassifiable after coder review, pathology report mention of inadequate specimen quality was the most common reason why a more detailed subtype could not be assigned. Less than 10% of pathology reports did not yield a detailed subtype because the pathologist considered the specimen truly unclassifiable. This proportion is lower than our prior finding of 25% of lymphoma NOS cases considered as unclassifiable after microscopic re-review by an expert hematopathologist (21). Cases originally classified as NOS varied with respect to age, geography, and particularly evidence of AIDS, and the distributions of subtypes for "resolved" NOS cases varied from the expected distribution. These variations, coupled with the high prevalence of NOS lymphomas, which represented about one in five of all NHLs reported to the Surveillance, Epidemiology, and End Results program, suggest that the misclassification of classifiable lymphomas as NOS may have biased prior Surveillance, Epidemiology, and End Results data-based assessments of NHL subtype-specific incidence and survival (25-29). Therefore, the surveillance of lymphoma subtypes could be improved by routine secondary editing or review of histologic coding by cancer registry personnel for all lymphomas initially reported as NOS.

Between the 1988 to 1994 and 1998 to 2000 study groups, which were chosen to differ temporally in relation to the adoption of the REAL and WHO classification schemes, we observed only subtle differences in overall or subtype-specific agreement for the most part. Overall agreement of computer-assigned and re-reviewed ICD-O-3 code was identical (77%) in both groups, as was the proportion of resolvable NOS cases (42-43%). For specific subtype groupings, agreement did seem to improve over time for the mantle cell, lymphoplasmacytic, and some of the T-cell lymphoma groups but was comparable for most other subtype groupings. In addition, completeness of the malignant cell type variable improved from 32% to 64% between the two study time periods.

Several factors may affect the generalizability of our findings. First, lymphoma subtype distributions in the San Francisco Bay Area generally differ from those in other regions during the study years, particularly with respect to HIV-associated lymphomas. The higher incidence of these lymphomas may influence local classification practices (e.g., classification of central nervous system lymphomas as NOS). However, reasons for NOS classification did not vary significantly between patients with and without AIDS, although a slightly higher percentage of AIDS lymphoma patients (21% versus 15%) were classified as NOS because "assay information was not available" from the pathology report, suggesting differences in diagnostic procedures for HIV and non–HIV-associated lymphomas. Second, we delineated our case series according to ICD-O-2–defined codes for lymphomas and thereby did not include cases originally coded as leukemias or other lymphoid neoplasms in our case series. Thus, our data cannot speak well to the reliability of codes for lymphoma entities with leukemic presentations (e.g., 9820). Third, for the 1998 to 2000 study group, we were unable to obtain a substantial proportion of pathology reports requested from hospitals. As much of this nonparticipation occurred at the hospital rather than patient level, our final study group might be of biased representation with respect to pathologist diagnostic or cancer registrar coding practices that differ among hospitals irrespective of their teaching status. This effect is probably minor, as histologic subtype distributions were generally comparable between the participating and nonparticipating groups, with only a slightly greater proportion of large B-cell lymphomas (ICD-O-3 code 9680) in the participating group.

The dissemination of the consensus REAL/WHO classification system marked a hopeful moment in our quest to learn more about the etiologies of specific lymphoma subtypes, especially subtypes shown to be increasing in incidence. However, as tracking of lymphoma subtype trends over time remains an important activity, more research should be done to understand and implement reliable means of consistent subtype classification over time in cancer registry and other data. Ensuring that uniform means of subtype classification and grouping are being used in all future surveillance and etiologic studies of lymphoid neoplasms is an explicit goal of InterLymph, the International Lymphoma Epidemiology Consortium (30). Although the REAL/WHO represents the most reliable classification system devised thus far, ongoing improvements in molecular characterization of lymphoid neoplasms will surely lead to even better classification schemes that may further enlighten the etiologies of these cancers.

	Acknowledgments

 
We thank Elizabeth Traynor, M.D.; Paige Bracci; Jennifer Kristianson; Kathleen Torres; and Jennifer Yang for their contributions.

	Footnotes

 
Grant support: Rapid Response Surveillance Study program of the National Cancer Institute Surveillance Epidemiology and End Results program contract N01-CN-65107. National Cancer Institute grants CA45614, CA66529, and CA89745 (E.A. Holly) supported the primary work on the case-control study that collected the pathology reports for the 1988 to 1994 group. Cancer registry data were collected by the Northern California Cancer Center under contract N01-CN-65107 with the National Cancer Institute, NIH and with the support of the California Cancer Registry, a project of the Cancer Surveillance Section, California Department of Health Services, under subcontract 1006128 with the USPHS.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Note: The content of this publication does not necessarily reflect the views or policies of the U.S. Department of Health and Human Services nor the California Department of Health Services, nor does mention of trade names, commercial products, or organizations imply endorsement by the U.S. government or State of California.

Received 7/27/05; revised 1/11/06; accepted 1/31/06.

	References

Top Abstract Introduction Materials and Methods Results Discussion References

 

1. Surveillance, Epidemiology, and End Results (SEER) Program Public-Use Data (1973–2002), released April 2005, based on the November 2004 submission. Silver Spring (MD): Information Management Services, Inc.
2. Harris NL, Jaffe ES, Stein H, et al. A revised European-American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group. Blood 1994;84:1361–92.[Free Full Text]
3. Percy C, Van Holten V, Muir C. International classification of diseases for oncology. Geneva: WHO; 1990.
4. Fritz A, Percy C, Jack A, et al., editors. International Classification of Diseases for Oncology, 3rd ed. Geneva: WHO; 2000.
5. Percy C, Fritz A, Ries L, editors. Conversion of neoplasms by topography and morphology from the International Classification of Diseases for Oncology, 2nd ed. to the International Classification of Diseases for Oncology, 3rd ed. Rockville (MD): National Cancer Institute; 2001.
6. Harris NL, Jaffe ES, Diebold J, et al. World Health Organization classification of neoplastic diseases of the hematopoietic and lymphoid tissues: report of the Clinical Advisory Committee meeting-Airlie House, Virginia, November 1997. J Clin Oncol 1999;17:3835–49.[Abstract/Free Full Text]
7. International Lymphoma Study Group. A clinical evaluation of the International Lymphoma Study Group classification of non-Hodgkin's lymphoma. The Non-Hodgkin's Lymphoma Classification Project. Blood 1997;89:3909–18.[Abstract/Free Full Text]
8. Holly EA, Lele C, Bracci P. Non-Hodgkin's lymphoma in homosexual men in the San Francisco Bay Area: occupational, chemical, and environmental exposures. J Acquir Immune Defic Syndr Hum Retrovirol 1997;15:223–31.[Medline]
9. Holly EA, Lele C. Non-Hodgkin's lymphoma in HIV-positive and HIV-negative homosexual men in the San Francisco Bay Area: allergies, prior medication use, and sexual practices. J Acquir Immune Defic Syndr Hum Retrovirol 1997;15:211–22.[Medline]
10. Holly EA, Lele C, Bracci PM. Hair-color products and risk for non-Hodgkin's lymphoma: a population-based study in the San Francisco bay area. Am J Public Health 1998;88:1767–73.[Abstract/Free Full Text]
11. Holly EA, Lele C, Bracci PM, et al. Case-control study of non-Hodgkin's lymphoma among women and heterosexual men in the San Francisco Bay Area, California. Am J Epidemiol 1999;150:375–89.[Abstract/Free Full Text]
12. Kamel OW, Holly EA, van de Rijn M, et al. A population based, case control study of non-Hodgkin's lymphoma in patients with rheumatoid arthritis. J Rheumatol 1999;26:1676–80.[Medline]
13. Tiirikainen MI, Mullaney BP, Holly EA, et al. DNA copy number alterations in HIV-positive and HIV-negative patients with diffuse large-cell lymphomas. J Acquir Immune Defic Syndr 2001;27:272–6.[Medline]
14. Holly EA, Gautam M, Bracci PM. Comparison of interviewed and non-interviewed non-Hodgkin's lymphoma (NHL) patients in the San Francisco Bay Area. Ann Epidemiol 2002;12:419–25.[CrossRef][Medline]
15. Chow EJ, Holly EA. Blood transfusions as a risk factor for non-Hodgkin's lymphoma in the San Francisco Bay Area: a population-based study. Am J Epidemiol 2002;155:725–31.[Abstract/Free Full Text]
16. Holly EA, Bracci PM. San Francisco population-based study of non-Hodgkin's lymphoma histology and medical history among HIV-negative participants. Am J Epidemiol 2003;158:316–27.[Abstract/Free Full Text]
17. Bracci PM, Holly EA. Tobacco use and non-Hodgkin lymphoma: results from a population-based case-control study in the San Francisco Bay Area, California. Cancer Causes Control 2005;16:333–46.[Medline]
18. Holly EA, Eberle CA, Bracci PM. Prior history of allergies and pancreatic cancer in the San Francisco Bay area. Am J Epidemiol 2003;158:432–41.[Abstract/Free Full Text]
19. Holly EA, Bracci PM. Population-based study of non-Hodgkin lymphoma, histology, and medical history among human immunodeficiency virus-negative participants in San Francisco. Am J Epidemiol 2003;158:316–27.[Abstract/Free Full Text]
20. Skibola CF, Forrest MS, Coppede F, et al. Polymorphisms and haplotypes in folate-metabolizing genes and risk of non-Hodgkin lymphoma. Blood 2004;104:2155–62.[Abstract/Free Full Text]
21. Clarke CA, Glaser SL, Dorfman RF, et al. Expert review of non-Hodgkin's lymphomas in a population-based cancer registry: reliability of diagnosis and subtype classifications. Cancer Epidemiol Biomarkers Prev 2004;13:138–43.[Abstract/Free Full Text]
22. Hennekens CH, Buring JE. Epidemiology in medicine. Boston: Little, Brown and Company; 1987.
23. Dick F, VanLier S, Banks P, et al. Use of the working formulation for non-Hodgkin's lymphoma in epidemiologic studies: agreement between reported diagnoses and a panel of experienced pathologists. J Natl Cancer Inst 1987;78:1137–44.[Medline]
24. Turner JJ, Hughes AM, Kricker A, et al. Use of the WHO lymphoma classification in a population-based epidemiological study. Ann Oncol 2004;15:631–7.[Abstract/Free Full Text]
25. Greiner TC, Medeiros LJ, Jaffe ES. Non-Hodgkin's lymphoma. Cancer 1995;75:370–80.[CrossRef][Medline]
26. Herrinton LJ. Epidemiology of the Revised European-American Lymphoma Classification subtypes. Epidemiol Rev 1998;20:187–203.[Free Full Text]
27. Groves FD, Linet MS, Travis LB, et al. Cancer surveillance series: non-Hodgkin's lymphoma incidence by histologic subtype in the United States from 1978 through 1995. J Natl Cancer Inst 2000;92:1240–51.[Abstract/Free Full Text]
28. Eltom MA, Jemal A, Mbulaiteye SM, et al. Trends in Kaposi's sarcoma and non-Hodgkin's lymphoma incidence in the United States from 1973 through 1998. J Natl Cancer Inst 2002;94:1204–10.[Abstract/Free Full Text]
29. Ries LAG, Eisner MP, Kosary CL, et al., editors. SEER cancer statistics review, 1973–2002. Bethesda (MD): National Cancer Institute; 2005.
30. Boffetta P, Linet M, Armstrong B. The Interlymph collaboration: a consortium of molecular epidemiologic studies of non-Hodgkin's lymphoma [abstract 1579]. Proc Am Assoc Cancer Res 2003;44:308.

This article has been cited by other articles:

				L. M. Morton, J. J. Turner, J. R. Cerhan, M. S. Linet, P. A. Treseler, C. A. Clarke, A. Jack, W. Cozen, M. Maynadie, J. J. Spinelli, et al. Proposed classification of lymphoid neoplasms for epidemiologic research from the Pathology Working Group of the International Lymphoma Epidemiology Consortium (InterLymph) Blood, July 15, 2007; 110(2): 695 - 708. [Abstract] [Full Text] [PDF]

				J. R. Cerhan, S. Wang, M. J. Maurer, S. M. Ansell, S. M. Geyer, W. Cozen, L. M. Morton, S. Davis, R. K. Severson, N. Rothman, et al. Prognostic significance of host immune gene polymorphisms in follicular lymphoma survival Blood, June 15, 2007; 109(12): 5439 - 5446. [Abstract] [Full Text] [PDF]

				U. Lim, S. S. Wang, P. Hartge, W. Cozen, L. E. Kelemen, S. Chanock, S. Davis, A. Blair, M. Schenk, N. Rothman, et al. Gene-nutrient interactions among determinants of folate and one-carbon metabolism on the risk of non-Hodgkin lymphoma: NCI-SEER Case-Control Study Blood, April 1, 2007; 109(7): 3050 - 3059. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Clarke, C. A. Articles by Holly, E. A. Search for Related Content PubMed PubMed Citation Articles by Clarke, C. A. Articles by Holly, E. A.