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Risk of Leukemia After Dengue Virus Infection Published OnlineFirst February 12, 2020; DOI: 10.1158/1055-9965.EPI-19-1214 CANCER EPIDEMIOLOGY, BIOMARKERS & PREVENTION | RESEARCH ARTICLE Risk of Leukemia after Dengue Virus Infection: A Population-Based Cohort Study Yu-Wen Chien1,2, Chia-Chun Wang3, Yu-Ping Wang1, Cho-Yin Lee4,5, and Guey Chuen Perng6,7,8 ABSTRACT ◥ Background: Infections account for about 15% of human cancers Results: We identified 12,573 patients with dengue and 62,865 globally. Although abnormal hematologic profiles and bone mar- non-dengue controls. Patients with dengue had a higher risk of row suppression are common in patients with dengue, whether leukemia [adjusted HR, 2.03; 95% confidence interval (CI), 1.16– dengue is associated with a higher risk of leukemia has not been 3.53]. Stratified analyses by different follow-up periods showed investigated. that dengue virus infection was significantly associated with a Methods: We conducted a nationwide population-based higher risk of leukemia only between 3 and 6 years after infection cohort study by analyzing the National Health Insurance (adjusted HR, 3.22; 95% CI, 1.25–8.32). There was no significant Research Databases in Taiwan. Laboratory-confirmed dengue association between dengue and the risk of other cancers. patients between 2002 and 2011 were identified; five matched Conclusions: This study provides the first epidemiologic non-dengue controls were randomly selected for each patient. evidence for the association between dengue virus infection and Follow-up ended on December 31, 2015. Multivariate Cox leukemia. proportional hazard regression models were used to evaluate Impact: Considering the rapidly increasing global incidence of the effect of dengue virus infection on the risk of leukemia. dengue and the burden of leukemia, further studies are required Cancers other than leukemia were used as falsification endpoints to verify this association and to unravel the potential mechanisms to evaluate the validity of this study. of pathogenesis. Introduction carcinoma caused by hepatitis virus B or hepatitis virus C, cervical cancer caused by human papillomavirus, nasopharyngeal carcinoma According to recent statistics, there are approximately 17.2 million caused by Epstein–Barr virus, and Kaposi sarcoma caused by human new cancer cases and 8.9 million cancer-related deaths worldwide per herpesvirus-8 are all well-known infection-attributable cancers (2). year (1). Among them, infections account for about 15% of human For hematologic malignancies, examples of such causal relationships cancer cases (2). Several pathogens have been recognized by the include those between human T-cell leukemia virus type I and adult International Agency for Research on Cancer as Group 1 carcinogens, T-cell leukemia, Epstein–Barr virus and Burkitt lymphoma and which mean that there is sufficient evidence of carcinogenicity in Hodgkin lymphoma, human immunodeficiency virus and Hodgkin humans or there is both strong evidence in exposed humans that the lymphoma and non-Hodgkin lymphoma, hepatitis C virus and non- agent exhibits key characteristics of carcinogens and sufficient evi- Hodgkin lymphoma, and Helicobacter pylori and gastric mucosa- dence of carcinogenicity in experimental animals (3). Hepatocellular associated lymphoid tissue lymphoma (2). Dengue fever is an important mosquito-borne infectious disease (4). 1Department of Public Health, College of Medicine, National Cheng Kung Over the past decades, the incidence of dengue has dramatically University, Tainan, Taiwan. 2Department of Occupational and Environmental increased worldwide with significant geographical expansion to new Medicine, National Cheng Kung University Hospital, College of Medicine, Nation- countries and regions, which probably results from rapid urbanization, al Cheng Kung University, Tainan, Taiwan. 3Division of Radiation Oncology, increasing frequency of travel, and global climate change (5). An Department of Oncology, National Taiwan University Hospital, Taipei, Taiwan. estimated 390 million people are infected by dengue virus every year, of 4Department of Biomedical Engineering, National Yang-Ming University, Taipei, 5 which 25% are symptomatic (5, 6). Taiwan. Department of Radiation Oncology, Taoyuan General Hospital, Ministry fi of Health and Welfare, Taoyuan City, Taiwan. 6Institute of Basic Medical Abnormal hematologic pro les, such as leukopenia, thrombocyto- Sciences, College of Medicine, National Cheng Kung University, Tainan, Taiwan. penia, and atypical lymphocytes, are hallmark laboratory findings in 7Department of Microbiology and Immunology, College of Medicine, National patients with dengue (5). Bone marrow suppression is also commonly Cheng Kung University, Tainan, Taiwan. 8Center of Infectious Disease and observed in patients with dengue in the early stage of infection (7–9). Signaling Research, National Cheng Kung University, Tainan, Taiwan. Moreover, dengue virus can be recovered from bone marrows of both Note: Supplementary data for this article are available at Cancer Epidemiology, fatal and survival human subjects (10). In-line with these clinical Biomarkers & Prevention Online (http://cebp.aacrjournals.org/). observations, cumulative laboratory evidence suggests that hemato- Corresponding Authors: Guey Chuen Perng, Department of Microbiology and poietic progenitor cells in bone marrow, in both in vitro and ex vivo Immunology, College of Medicine, National Cheng Kung University, No. 1, systems, as well as in vivo nonhuman primates, are highly infectable University Road, Tainan 70101, Taiwan. Phone: 886-6235-3535, ext. 5626; by dengue virus (11–15). Furthermore, case reports of acute myeloid Fax: 886-6236-9233; E-mail: [email protected]; and Cho-Yin Lee, leukemia precipitated by dengue virus infection (16) and dengue virus Department of Biomedical Engineering, National Yang-Ming University, No. – 155, Section 2, Linong Street, Beitou District, Taipei City 112, Taiwan. Phone: 8862- infection mimicking plasma cell leukemia (17) have been documen- 2826-7000, ext. 5368; Fax: 8862-2821-0847; E-mail: [email protected] ted. These clues guided us to hypothesize that dengue virus infection might be associated with leukemia. Cancer Epidemiol Biomarkers Prev 2020;XX:XX–XX Here we investigated whether the risk of leukemia was increased doi: 10.1158/1055-9965.EPI-19-1214 after dengue virus infection by analyzing nationwide population Ó2020 American Association for Cancer Research. databases in Taiwan. In dengue hyperendemic countries, most of the AACRJournals.org | OF1 Downloaded from cebp.aacrjournals.org on September 28, 2021. © 2020 American Association for Cancer Research. Published OnlineFirst February 12, 2020; DOI: 10.1158/1055-9965.EPI-19-1214 Chien et al. people have been infected by dengue virus multiple times (18), making urbanized according to Liu and colleagues (22). Because only a small the selection of uninfected people for comparison challenging. The percentage of people lived in levels four to seven, we combined these availability of comprehensive nationwide databases (19, 20), as well as four levels into a single urbanization stratum, we referred to as level 4. the low incidence of dengue in Taiwan provided us unique and The monthly income was classified into three levels (unemployed, low, valuable resources to test this hypothesis. and high). Several lifestyle-related diseases, including chronic obstruc- tive pulmonary disease (COPD), hypertension, hyperlipidemia, dia- betes mellitus, and peptic ulcer disease, were considered as potential Materials and Methods confounders. These comorbidities for each subject were defined as at Data sources and study population least three outpatient visits or one hospital admission with relevant A population-based cohort study was conducted by analyzing the ICD-9-CM codes (Supplementary Table S2) between January 1, 2000 National Health Insurance Research Databases (NHIRD) and the and the index date. Notifiable Disease Dataset of Confirmed Cases (19). The former database contains detailed medical insurance claims from the National Statistical analysis Health Insurance (NHI) program, which covers >99.6% of the total The baseline characteristics between dengue and non-dengue population of over 23 million in Taiwan (19). All information for each groups were compared using standardized mean differences, and a person in NHIRD was linked through an encrypted unique personal meaningful difference between groups was considered when the identification number, which also allowed linkage to multiple national standardized mean difference was greater than 0.1 (23). The incidence databases including registries of birth, deaths, and reportable infec- rate of leukemia was calculated as the number of patients diagnosed tious diseases (19, 20). In Taiwan, reporting suspected patients with during follow-up divided by total follow-up time in person-year for dengue is mandatory by law. Blood samples from suspected cases both groups (24). We constructed multivariable Cox proportional should be tested by certified laboratories approved by the Taiwan hazard regression models to estimate HRs and 95% confidence inter- Centers for Disease Control to confirm the diagnosis of dengue during vals (CI) for leukemia among dengue virus–infected people compared the study period. The laboratory criteria for confirmed dengue infec- with uninfected people, adjusting for potential confounders as tion evolved over the study period but generally included the following: listed above. The proportional hazard assumption was checked by (i)
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