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Environment-Wide Association Study of CKD

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Environment-Wide Association Study of CKD CJASN ePress. Published on May 22, 2020 as doi: 10.2215/CJN.06780619 Article Environment-Wide Association Study of CKD Jeonghwan Lee ,1 Sohee Oh,2 Habyeong Kang ,3 Sunmi Kim ,3 Gowoon Lee,3 Lilin Li ,4 Clara Tammy Kim,5 Jung Nam An,6 Yun Kyu Oh ,1,4 Chun Soo Lim,1,4 Dong Ki Kim,4,7 Yon Su Kim,4,7 Kyungho Choi,3 and Jung Pyo Lee 1,4 Abstract Background and objectives Exposure to environmental chemicals has been recognized as one of the possible contributors to CKD. We aimed to identify environmental chemicals that are associated with CKD. 1Department of Internal Medicine, Design, setting, participants, & measurements We analyzed the data obtained from a total of 46,748 adults who Seoul National participated in the National Health and Nutrition Examination Survey (1999–2016). Associations of chemicals University Boramae measured in urine or blood (n5262) with albuminuria (urine albumin-to-creatinine ratio $30 mg/g), reduced Medical Center, Seoul, eGFR(,60 ml/min per 1.73 m2), and a composite of albuminuria or reduced eGFR were tested and validated using Republic of Korea 2Medical Research the environment-wide association study approach. Collaborating Center, Seoul National Results Among 262 environmental chemicals, seven (3%) chemicals showed significant associations with University Boramae increased risk of albuminuria, reduced eGFR, or the composite outcome. These chemicals included metals and Medical Center, Seoul, Republic of Korea other chemicals that have not previously been associated with CKD. Serum and urine cotinines, blood 2,5- 3 Department of dimethylfuran (a volatile organic compound), and blood cadmium were associated with albuminuria. Blood lead Environmental Health and cadmium were associated with reduced eGFR. Blood cadmium and lead and three volatile compounds (blood Sciences, School of 2,5-dimethylfuran,blood furan,andurinary phenylglyoxylicacid) were associatedwiththecompositeoutcome.A Public Health, Seoul total of 23 chemicals, including serum perfluorooctanoic acid, seven urinary metals, three urinary arsenics, urinary National University, Seoul, Republic of nitrate and thiocyanate, three urinary polycyclic aromatic hydrocarbons, and seven volatile organic compounds, Korea were associated with lower risks of one or more manifestations of CKD. 4Department of Internal Medicine, Seoul Conclusions A number of chemicals were identified as potential risk factors for CKD among the general National University population. College of Medicine, Seoul, Republic of CJASN 15: ccc–ccc, 2020. doi: https://doi.org/10.2215/CJN.06780619 Korea 5Institute of Life and Death Studies, Hallym University, Chuncheon, Introduction (13). In some populations, other environmental chem- – Republic of Korea CKD is a global public health problem (1 3). The high icals, including perfluoroalkyl acids, dioxins, poly- 6Department of Internal prevalence of CKD worldwide cannot solely be cyclic aromatic hydrocarbons, and polychlorinated Medicine, Hallym explained by well known causes such as diabetes biphenyls, have been suggested as a new risk factors University Sacred Heart mellitus, hypertension, and GN. Recently, environ- Hospital, Anyang, for CKD (14,15). However, the associations of these Republic of Korea mental factors have been recognized as important risk environmental chemicals with kidney disease param- 7Department of Internal factors for the development and progression process eters and CKD are not consistent according to the time Medicine, Seoul of CKD (4,5). Production and use of consumer points, populations, and clinical circumstances. In National University chemicals have significantly increased in recent de- Hospital, Seoul, addition, our knowledge on the role of chemicals in Republic of Korea cades (6), and chemicals can cause adverse outcomes the cause of CKD is quite limited, considering the for human health (7,8). Epidemiologic studies have growing number of chemicals being introduced in the Correspondence: revealed that at the levels of current exposure, many market and used in daily lives. Dr. Jung Pyo Lee, chemicals are closely associated with human diseases, In this study, the associations between various Department of Internal including neurologic, endocrinologic, and neoplastic environmental chemicals measured in the general Medicine, Seoul National University diseases (9,10). United States population and the prevalence of Boramae Medical Various genetic and environmental factors are CKD were evaluated. For this purpose, a genome- Center and Seoul suggested as potential risk factors for developing wide association study methodology was applied for National University CKD (11). Indeed, several environmental chemicals, environmental chemicals instead of various genetic College of Medicine, 20 Boramae-ro 5-gil, including melamine and heavy metals like lead or phenotypes, i.e., an environment-wide association Dongjak-gu, Seoul cadmium, have long been known to be risk factors for study (EWAS) (16). By utilizing EWAS, hundreds of 07061, Republic of kidney injury and CKD (12). Recently, consumer bio-monitored chemicals were tested simultaneously Korea. Email: chemicals such as phthalates and bisphenol A have for their association with CKD. The results of this nephrolee@ gmail.com also been reported to be associated with CKD not only study will help to identify a list of potential chemicals among adults, but also among children or adolescents with significant association with CKD, which can be www.cjasn.org Vol 15 June, 2020 Copyright © 2020 by the American Society of Nephrology 1 2 CJASN further confirmed in follow-up epidemiologic studies and Statistical Analyses experimental mechanistic investigations. The associations between various environmental chem- icals measured in the urine or blood, and CKD were assessed by the EWAS approach proposed by Patel et al. for Materials and Methods type2diabetesmellitus(16,20).EWASreferstothe association study of various exposomes and disease out- Study Participants and Data Analyzed We analyzed 46,748 adults (age $18 years) who partic- comes similarly to a genome-wide association study of SNPs and disease. In general, an EWAS of environmental ipated in the National Health and Nutrition Examination fi Survey (NHANES) from 1999 to 2016. Among 92,062 chemicals for speci c disease requires a multiple-cycle eligible participants, 38,714 young individuals (age ,18 population study such as NHANES. An EWAS integrates years) were initially excluded. In addition, 6600 partici- the multiple survey results between chemical and disease pants who did not have data for either urinary albumin-to- using meta-analysis methods, and validates the results creatinine ratio (ACR) or eGFR were finally excluded. This using other populations. Figure 1 presents the outline of the cross-sectional, observational cohort study was approved analytic approach used in this study. – by the Institutional Review Board of Seoul National We utilized the nine NHANES surveys (1999 2016) to University Boramae Medical Center (approval number analyze the association between environmental chemicals 07–2019–16). Information on the environmental chemicals and CKD. The data sets from nine NHANES cycles – as well as demographic and laboratory data were obtained (1999 2016) during the 18-year period were divided into from the NHANES database (https://www.cdc.gov/ the discovery and the validation sets. To reduce errors nchs/nhanes/index.htm; demographic, examination, derived from chronological order, we assigned cycles in an – questionnaire, and laboratory data set) in March 2019. alternate manner into the discovery set (1999 2000, – – – – We defined hypertension as an average systolic BP of 2003 2004, 2007 2008, 2011 2012, and 2015 2016) and – – – .140 mm Hg or diastolic BP of .90 mm Hg measured at validation set (2001 2002, 2005 2006, 2009 2010, and – least twice, history of hypertension, or currently taking 2013 2014). In the discovery set, which is composed of fi antihypertensive medications. Diabetes mellitus was de- data from the ve NHANES cycles, the association be- fined as fasting glucose level of .126 mg/dl, random tween each environmental chemical and CKD was tested glucose level of .200 mg/dl, or history of diabetes through survey weighted logistic regression with covari- mellitus. Corrected serum creatinine levels were used in ates of age, age-squared, sex, diabetes mellitus, hyperten- the survey of 1999–2000 and 2005–2006 (17,18). Serum and sion,bodymassindex,race/ethnicity,smoking,and urine creatinine levels were measured using the Jaffe rate socioeconomic status. Family poverty-to-income ratio as methods (kinetic alkaline picrate) with calibration to an a continuous variable was used for socioeconomic status isotope dilution mass spectrometry reference method. adjustment. Considering the wide range of ages among Urinary albumin levels were measured using solid-phase NHANES participants, we added the age-squared term as a fluorescent immunoassay. We calculated eGFR using the covariate to model the nonlinear effect of differing ages on CKD Epidemiology Collaboration equations (19). Three disease outcomes. Imputation of missing values was not CKD outcomes were assessed: albuminuria (urinary ACR considered. The appropriate sample weights of the smallest ratio $30 mg/g), reduced eGFR (,60 ml/min per 1.73 m2), subpopulation among variables were selected and adjusted and a composite outcome of albuminuria or reduced eGFR. among weights of mobile examination center or subsample weights of each chemicals (21). Then, the estimates from
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