Estimating missing concentrations of p,p′-DDT in the 1999–2004 National Health and Nutrition Examination Survey using multiple imputation

  • Charles J. EverettEmail author
  • Mulugeta Gebregziabher
Research Article


We investigated the association between diabetes and p,p′-DDT (dichlorodiphenyltrichloroethane) in blood of Mexican Americans who participated in the 1999–2004 National Health and Nutrition Examination Survey (NHANES). In this sample, p,p′-DDT were missing in 50% of subjects and we used multiple imputation (MI) to address the problem. Compared to ignoring the missing data, MI led to a more robust threshold for the p,p′-DDT reference category. Whereas previously p,p′-DDT ≤ 0.0860 ng/g was used as the reference category, using MI, we were able to use p,p′-DDT < 0.0574 ng/g as the reference category to study the association between p,p′-DDT and diabetes via logistic regression. In this analysis, p,p′-DDT ≥ 0.0750 ng/g was associated with an odds ratio of 1.99 (95% CI 1.09–3.61) for diabetes and 4.20 (95% CI 1.93–9.12) for diabetic nephropathy. The reference category for diabetes without nephropathy outcome stayed consistent after MI but our analysis confirmed that p,p′-DDT > 0.0860 ng/g was associated with diabetes without nephropathy with an odds ratio of 1.89 (95% CI 1.09–3.27). Our study showed that MI can be effectively used to deal with missing at random data in persistent organic pollutants measured in the 1999–2004 NHANES.


DDT (dichlorodiphenyltrichloroethane) Diabetes Kidney disease Diabetic nephropathy Mexican American NHANES (National Health and Nutrition Examination Survey) Multiple imputation 


Supplementary material

11356_2018_4078_MOESM1_ESM.pdf (101 kb)
ESM 1 (PDF 101 kb)


  1. Berglund PA (2010) An introduction to multiple imputation of complex sample data using SAS v9.2. SAS Global Forum 2010; Paper 265-2010, pp 1–12Google Scholar
  2. Centers for Disease Control and Prevention (CDC) (2018) National Center for Health Statistics. National Health and Nutrition Examination Survey, NHANES 1999–2004. Accessed 19 Nov 2018
  3. Cox S, Niskar AS, Narayan KM, Marcus M (2007) Prevalence of self-reported diabetes and exposure to organochlorine pesticides among Mexican Americans: Hispanic Health and Nutrition Examination Survey, 1982-1984. Environ Health Perspect 115:1747–1752CrossRefGoogle Scholar
  4. Eskenazi B, Chevrier J, Rosas LG, Anderson HA, Bornman MS, Bouwman H, Chen A, Cohn BA, de Jager C, Henshel DS, Leipzig F, Leipzig JS, Lorenz EC, Snedeker SM, Stapleton D (2009) The Pine River statement: human health consequences of DDT use. Environ Health Perspect 117:1359–1367CrossRefGoogle Scholar
  5. Evangelou E, Ntritsos G, Chondrogiorgi M, Kavvoura FK, Hernandez AF, Ntzani EE, Tzoulaki I (2016) Exposure to pesticides and diabetes: a systematic review and meta-analysis. Environ Int 91:60–68CrossRefGoogle Scholar
  6. Everett CJ, Thompson OM (2015) Association of DDT and heptachlor epoxide in human blood with diabetic nephropathy. Rev Environ Health 30:93–97CrossRefGoogle Scholar
  7. Everett CJ, Thompson OM, Dismuke CE (2017a) Exposure to DDT and diabetic nephropathy among Mexican Americans in the 1999-2004 National Health and Nutrition Examination Survey. Environ Pollut 222:132–137CrossRefGoogle Scholar
  8. Everett CJ, Thompson OM, Dismuke CE (2017b) DDT and DDE concentrations in blood of Mexican Americans exposed to DDT in Mexico: the 1999-2004 National Health and Nutrition Examination Survey. Int J Agric Environ Res 3(4):370–376Google Scholar
  9. Gillespie BW, Chen Q, Reichert H, Franzblau A, Hedgeman E, Lepkowski J, Adriaens P, Demond A, Luksemburg W, Garabrant DH (2010) Estimating population distributions when some data are below a limit of detection by using a reverse Kaplan-Meier estimator. Epidemiology 21(Suppl. 4):S64–S70CrossRefGoogle Scholar
  10. Jones RM, Stayner LT, Demirtas H (2014) Multiple imputation for assessment of exposures to drinking water contaminants: evaluation with the Atrazine Monitoring Program. Environ Res 134:466–473CrossRefGoogle Scholar
  11. Little RJA, Rubin DB (2002) Statistical analysis with missing data, 2nd edn. Wiley, HobokenCrossRefGoogle Scholar
  12. Lopez-Carrillo L, Torres-Sanchez L, Moline J, Ireland K, Wolff MS (2001) Breast-feeding and serum p,p’-DDT levels among Mexican women of childbearing age: a pilot study. Environ Res 87:131–135CrossRefGoogle Scholar
  13. Smith D (1999) Worldwide trends in p,p’-DDT levels in human breast milk. Int J Epidemiol 28:179–188CrossRefGoogle Scholar
  14. Turnbull BW (1976) The empirical distribution function with arbitrarily grouped, censored, and truncated data. J R Stat Soc Ser B 38:290–295Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Public Health SciencesMedical University of South CarolinaCharlestonUSA

Personalised recommendations