Abstract
The Michigan Long-Term PBB Study was established following exposure to polybrominated biphenyls (PBBs) in the early 1970s. Serum samples from cohort members were analyzed for PBB during 1976–1993. More than 20 years following this industrial incident, some participants still had measurable serum PBB concentration levels. Thus, there is continuing interest in understanding the elimination of PBB from the body. In the present study, we estimated serum PBB decay and investigated the effects of covariates on serum PBB decay rates among 406 female cohort members. We developed a decay model using a general linear mixed model, which attributes unique intercept and slope estimates for each individual while borrowing information across individuals for predicting these quantities. Age at exposure and body mass index (BMI) at the initial measurement were time-independent covariates. Time since exposure, smoking history, pregnancy status, and breast-feeding status were time-dependent covariates. Higher BMI was associated with a slower decay rate; smokers had a faster decay rate than nonsmokers; and increasing age at exposure was marginally associated with a slower decay rate. Our results suggest a faster serum PBB decay rate for women who breast-fed during the interval between serum PBB measurements. To evaluate the predictive performance of our modeling approach, we compared the results from this model with those from a previously developed ordinary least squares (OLS) two-stage decay model. The mixed-effects decay model predicted the observed serum PBB concentration levels significantly better than the OLS two-stage decay model (mixed-effects model, r=0.93; OLS two-stage model, r=0.86; P<0.0001).
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 6 print issues and online access
$259.00 per year
only $43.17 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Abbreviations
- BMI:
-
body mass index
- MDCH:
-
Michigan Department of Community Health
- MFHS:
-
Michigan Female Health Study
- MSE:
-
mean squared error
- OLS:
-
ordinary least squares
- PBB:
-
polybrominated biphenyl
- PCB:
-
polychlorinated biphenyl
- ppb:
-
parts per billion
References
Akaike H. A new look at the statistical model identification. IEEE Trans Automat Control 1974: 19 (6): 716–723.
Anderson H.A., and Wolff M.S. Environmental contaminants in human milk. J Expo Anal Environ Epidemiol 2000: 10 (6): 755–760.
ATSDR. Toxicological profile for Polybrominated Biphenyls and Polybrominated diphenyl ethers. In: Agency for Toxic Substances and Disease Registry, U.S. Department of Health and Human Services, Public Health Service, Atlanta, GA, USA, 2004.
Birnbaum L.S., and Staskal D.F. Brominated flame retardants: cause for concern? Environ Health Perspect 2004: 112 (1): 9–17.
Blanck H.M., Marcus M., Hertzberg V., Tolbert P.E., Rubin C., Henderson A.K., et al. Determinants of polybrominated biphenyl serum decay among women in the Michigan PBB cohort. Environ Health Perspect 2000a: 108 (2): 147–152.
Blanck H.M., Marcus M., Rubin C., Tolbert P.E., Hertzberg V.S., Henderson A.K., et al. Growth in girls exposed in utero and postnatally to polybrominated biphenyls and polychlorinated biphenyls. [see comment]. Epidemiology 2002: 13 (2): 205–210.
Blanck H.M., Marcus M., Tolbert P.E., Rubin C., Henderson A.K., Hertzberg V.S., et al. Age at menarche and tanner stage in girls exposed in utero and postnatally to polybrominated biphenyl. Epidemiology 2000b: 11 (6): 641–647.
Brock J.W., Burse V.W., Ashley D.L., Najam A.R., Green V.E., Korver M.P., et al. An improved analysis for chlorinated pesticides and polychlorinated biphenyls (PCBs) in human and bovine sera using solid-phase extraction. J Anal Toxicol 1996: 20 (7): 528–536.
Burse V.W., Needham L.L., Liddle J.A., Bayse D.D., and Price H.A. Interlaboratory comparison for results of analyses for polybrominated biphenyls in human serum. J Anal Toxicol 1980: 4 (1): 22–26.
Carter L.J. Michigans PBB incident—chemical mix-up leads to disaster. Science 1976: 192 (4236): 240–243.
Damstra T., Jurgelski Jr W., Posner H.S., Vouk V.B., Bernheim N.J., Guthrie J., et al. Toxicity of polybrominated biphenyls (PBBs) in domestic and laboratory animals. Environ Health Perspect 1982: 44: 175–188.
Davis S.I., Blanck H.M., Hertzberg V.S., Tolbert P.E., Rubin C., Cameron L.L., et al. Menstrual function among women exposed to polybrominated biphenyls: a follow-up prevalence study. Environmental Health: A Global Access Science Source 2005: 4: 15.
Eyster J.T., Humphrey H.E., and Kimbrough R.D. Partitioning of polybrominated biphenyls (PBBs) in serum, adipose tissue, breast milk, placenta, cord blood, biliary fluid, and feces. Arch Environ Health 1983: 38 (1): 47–53.
Flesch-Janys D., Becher H., Gurn P., Jung D., Konietzko J., Manz A., et al. Elimination of polychlorinated dibenzo-p-dioxins and dibenzofurans in occupationally exposed persons. J Toxicol Environ Health 1996: 47 (4): 363–378.
Fries G.F. The PBB episode in Michigan: an overall appraisal. Crit Rev Toxicol 1985: 16 (2): 105–156.
Hornung R.W., and Reed L.D. Estimation of average concentrations in the presence of nondetectable values. Appl Occup Environ Hyg 1990: 5 (1): 46–51.
Humphrey H., and Hayner N. Polybrominated biphenyls: an agricultural incident and its consequences: an epidemiological investigation of human exposure. Trace Substances in Environ Health 1976: 9: 57–63.
Humphrey H.E.B., Gardiner J.C., Pandya J.R., Sweeney A.M., Gasior D.M., McCaffrey R.J., et al. PCB congener profile in the serum of humans consuming Great Lakes fish. Environ Health Perspect 2000: 108 (2): 167–172.
Jacobson J.L., Fein G.G., Jacobson S.W., Schwartz P.M., and Dowler J.K. The transfer of polychlorinated biphenyls (PCBs) and polybrominated biphenyls (PBBs) across the human placenta and into maternal milk. Am J Public Health 1984: 74 (4): 378–379.
Jacobson J.L., Humphrey H.E., Jacobson S.W., Schantz S.L., Mullin M.D., and Welch R. Determinants of polychlorinated biphenyls (PCBs), polybrominated biphenyls (PBBs), and dichlorodiphenyl trichloroethane (DDT) levels in the sera of young children. Am J Public Health 1989: 79 (10): 1401–1404.
Kay K. Polybrominated biphenyls (PBB) environmental contamination in Michigan, 1973–1976. Environ Res 1977: 13 (1): 74–93.
Kreiss K., Roberts C., and Humphrey H.E. Serial PBB levels, PCB levels, and clinical chemistries in Michigan's PBB cohort. Arch Environ Health 1982: 37 (3): 141–147.
Kreuzer P.E., Csanady G.A., Baur C., Kessler W., Papke O., Greim H., et al. 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) and congeners in infants. A toxicokinetic model of human lifetime body burden by TCDD with special emphasis on its uptake by nutrition. Arch Toxicol 1997: 71 (6): 383–400.
Laird N.M., and Ware J.H. Random-effects models for longitudinal data. Biometrics 1982: 38 (4): 963–974.
Landrigan P.J., Wilcox Jr K.R., Silva Jr J., Humphrey H.E., Kauffman C., and Heath Jr C.W. Cohort study of Michigan residents exposed to polybrominated biphenyls: epidemiologic and immunologic findings. Ann N Y Acad Sci 1979: 320: 284–294.
Lin L.I.-K. A concordance correlation coefficient to evaluate reproducibility. Biometrics 1989: 45 (1): 255–268.
Littel R.C., Milliken G.A., Stroup W.W., and Wolfinger R.D. SAS System for Mixed Models. SAS Institute Inc., Cary, NC, USA, 1996.
Miceli J.N., Nolan D.C., Marks B., and Hariharan M. Persistence of polybrominated biphenyls (PBB) in human post-mortem tissue. Environ Health Perspect 1985: 60: 399–403.
Michalek J.E., Pirkle J.L., Caudill S.P., Tripathi R.C., Patterson Jr D.G., and Needham L.L. Pharmacokinetics of TCDD in veterans of operation ranch hand: 10-year follow-up. [erratum appears in J Toxicol Environ Health. 1997 26;52(6):557–558; PMID: 9424481]. J Toxicol Environ Health 1996: 47 (3): 209–220.
Najam A.R., Korver M.P., Williams C.C., Burse V.W., and Needham L.L. Analysis of a mixture of polychlorinated biphenyls and chlorinated pesticides in human serum by column fractionation and dual-column capillary gas chromatography with electron capture detection. J AOAC Int 1999: 82 (1): 177–185.
Needham L.L., Burse V.W., and Price H.A. Temperature-programmed gas chromatographic determination of polychlorinated and polybrominated biphenyls in serum. J Assoc Off Anal Chem 1981: 64 (5): 1131–1137.
Price H.A., Welch R.L., Scheel R.H., and Warren L.A. Modified multiresidue method for chlordane, toxaphene, and polychlorinated-biphenyls in fish. Bull Environ Contam Toxicol 1986: 37 (1): 1–9.
Rogan W.J., Gladen B.C., McKinney J.D., Carreras N., Hardy P., Thullen J., et al. Polychlorinated biphenyls (PCBs) and dichlorodiphenyl dichloroethene (DDE) in human milk: effects on growth, morbidity, and duration of lactation. Am J Public Health 1987: 77 (10): 1294–1297.
Rosen D.H., Flanders W.D., Friede A., Humphrey H.E., and Sinks T.H. Half-life of polybrominated biphenyl in human sera. Environ Health Perspect 1995: 103 (3): 272–274.
SAS. SAS/STAT 9.1 User's Guide, Volumes 1–7 Sas Institute Inc., Cary, NC, USA, 2004.
Schisterman E.F., Whitcomb B.W., Louis G.M.B., and Louis T.A. Lipid adjustment in the analysis of environmental contaminants and human health risks. Environ Health Perspect 2005: 113 (7): 853–857.
Sjodin A, Jones RS, Focant JF, Lapeza C, Wang RY, McGahee 3rd EE, et al. Retrospective time-trend study of polybrominated diphenyl ether and polybrominated and polychlorinated biphenyl levels in human serum from the United States. Environ Health Perspect 2004: 112 (6): 654–658.
Steiger J.H. Tests for comparing elements of a correlation matrix. Psychol Bull 1980: 87 (2): 245–251.
Sweeney A.M., Symanski E., Burau K.D., Kim Y.J., Humphrey H.E., and Smithci M.A. Changes in serum PBB and PCB levels over time among women of varying ages at exposure. Environ Res 2001: 86 (2): 128–139.
Thomas A.R., Marcus M., Zhang R.H., Blanck H.M., Tolbert P.E., Hertzberg V., et al. Breast-feeding among women exposed to polybrominated biphenyls in Michigan. Environ Health Perspect 2001: 109 (11): 1133–1137.
Verbeke G, and Molenberghs G Linear Mixed Models for Longitudinal Data, 1st edn. Springer-Verlag, New York, 2000.
Wickizer T.M., and Brilliant L.B. Testing for polychlorinated biphenyls in human milk. Pediatrics 1981: 68 (3): 411–415.
Wolff M.S., Anderson H.A., and Selikoff I.J. Human tissue burdens of halogenated aromatic chemicals in Michigan. JAMA 1982: 247 (15): 2112–2116.
Wolff M.S., and Schecter A. Accidental exposure of children to polychlorinated biphenyls. Arch Environ Contam Toxicol 1991: 20 (4): 449–453.
Acknowledgements
This research was funded by the National Institute of Environmental Health Sciences, National Institutes of Health (Grants R01-ES08341, R01-ES012014, and R01-ES012458-01) and was supported by the Centers of Disease Control and Prevention cooperative agreement U39/CCU500392. We thank the staff and participants of the Michigan Long-Term PBB Study; Dr. Kevin Cavanagh and Michael O'Keefe of the Division of Chemistry and Toxicology, Bureau of Laboratories, Michigan Department of Community Health; the Michigan Department of Community Health for assistance in interpretation of PBB analytic methods and results; and Paige Tolbert, Carol Rubin and Alden Henderson for collaboration on the Michigan Female Health Study. The findings/conclusions in this article are those of the authors and do not necessarily represent the CDC.
Author information
Authors and Affiliations
Corresponding author
Additional information
This work was carried out in the Rollins School of Public Health, 1518 Clifton Road NE, Emory University, Atlanta Georgia 30322, USA.
Rights and permissions
About this article
Cite this article
Terrell, M., Manatunga, A., Small, C. et al. A decay model for assessing polybrominated biphenyl exposure among women in the Michigan Long-Term PBB Study. J Expo Sci Environ Epidemiol 18, 410–420 (2008). https://doi.org/10.1038/sj.jes.7500633
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/sj.jes.7500633
Keywords
This article is cited by
-
Thyroid hormone levels associate with exposure to polychlorinated biphenyls and polybrominated biphenyls in adults exposed as children
Environmental Health (2019)
-
A cohort study of the association between secondary sex ratio and parental exposure to polybrominated biphenyl (PBB) and polychlorinated biphenyl (PCB)
Environmental Health (2009)