Skip to main content
Top
Published in: Environmental Health and Preventive Medicine 1/2019

Open Access 01-12-2019 | Research article

Intra-individual variations of organophosphate pesticide metabolite concentrations in repeatedly collected urine samples from pregnant women in Japan

Authors: Keisuke Hioki, Yuki Ito, Naoko Oya, Shoji F. Nakayama, Tomohiko Isobe, Takeshi Ebara, Kanemitsu Shibata, Naomi Nishikawa, Kunihiko Nakai, Tomota Kamida, Jun Ueyama, Mayumi Sugiura-Ogasawara, Michihiro Kamijima

Published in: Environmental Health and Preventive Medicine | Issue 1/2019

Login to get access

Abstract

Background

Low-dose exposure to organophosphate (OP) insecticides during pregnancy may adversely affect neurodevelopment in children. To evaluate the OP exposure levels, single urine sampling is commonly adopted to measure the levels of dialkylphosphates (DAPs), common OP metabolites. However, the inter-day variations of urinary DAP concentrations within subjects are supposed to be large due to the short biological half-lives of the metabolites, and it is thus considered difficult to accurately assess OP exposure during pregnancy with single sampling. This study aimed to assess intra-individual variations of DAP concentrations and the reproducibility of the exposure dose categorization of OPs according to DAP concentration ranges in pregnant women in Japan.

Methods

Urine samples were collected from 62 non-smoking pregnant women (12–22 weeks of gestation) living in Aichi Prefecture, Japan. First morning void (FMV) and spot urine samples taken between lunch and dinner on the same day were collected on five different days during 2 weeks. The concentrations of DAP and creatinine in urine samples were measured using an ultra performance liquid chromatography with tandem mass spectrometry. Creatinine-adjusted and unadjusted concentrations were used for the intraclass correlation coefficient (ICC) calculations and surrogate category analyses.

Results

For all DAP metabolites, the creatinine-adjusted single ICCs exceeded 0.4, indicating moderate reliability. Overall, ICCs of spot urine samples taken in the afternoon were better than those taken as FMV. Surrogate category analyses showed that participants were categorized accurately into four exposure dose groups according to the quartile points.

Conclusion

This study indicated that a single urine sample taken in the afternoon may be useful in assessing OP exposure as long as the exposure is categorized into quartiles when conducting epidemiological studies in early to mid-pregnant women in Japan.
Appendix
Available only for authorised users
Literature
3.
go back to reference Ueyama J, Harada KH, Koizumi A, Sugiura Y, Kondo T, Saito I, et al. Temporal levels of urinary neonicotinoid and dialkylphosphate concentrations in Japanese women between 1994 and 2011. Environ Sci Technol. 2015;49:14522–8.CrossRef Ueyama J, Harada KH, Koizumi A, Sugiura Y, Kondo T, Saito I, et al. Temporal levels of urinary neonicotinoid and dialkylphosphate concentrations in Japanese women between 1994 and 2011. Environ Sci Technol. 2015;49:14522–8.CrossRef
4.
go back to reference Ueyama J, Saito I, Kondo T, Taki T, Kimata A, Saito S, et al. Urinary concentrations of organophosphorus insecticide metabolites in Japanese workers. Chemosphere. 2012;87:1403–9.CrossRef Ueyama J, Saito I, Kondo T, Taki T, Kimata A, Saito S, et al. Urinary concentrations of organophosphorus insecticide metabolites in Japanese workers. Chemosphere. 2012;87:1403–9.CrossRef
5.
go back to reference Eskenazi B, Bradman A, Castorina R. Exposures of children to organophosphate pesticides and their potential adverse health effects. Environ Health Perspect. 1999;107 Suppl 3:409–19.CrossRef Eskenazi B, Bradman A, Castorina R. Exposures of children to organophosphate pesticides and their potential adverse health effects. Environ Health Perspect. 1999;107 Suppl 3:409–19.CrossRef
6.
go back to reference Bouchard MF, Chevrier J, Harley KG, Kogut K, Vedar M, Calderon N, et al. Prenatal exposure to organophosphate pesticides and IQ in 7-year-old children. Environ Health Perspect. 2011;119:1189–95.CrossRef Bouchard MF, Chevrier J, Harley KG, Kogut K, Vedar M, Calderon N, et al. Prenatal exposure to organophosphate pesticides and IQ in 7-year-old children. Environ Health Perspect. 2011;119:1189–95.CrossRef
7.
go back to reference Marks AR, Harley K, Bradman A, Kogut K, Barr DB, Johnson C, et al. Organophosphate pesticide exposure and attention in young Mexican-American children: the CHAMACOS study. Environ Health Perspect. 2010;118:1768–74.CrossRef Marks AR, Harley K, Bradman A, Kogut K, Barr DB, Johnson C, et al. Organophosphate pesticide exposure and attention in young Mexican-American children: the CHAMACOS study. Environ Health Perspect. 2010;118:1768–74.CrossRef
8.
go back to reference Engel SM, Berkowitz GS, Barr DB, Teitelbaum SL, Siskind J, Meisel SJ, et al. Prenatal organophosphate metabolite and organochlorine levels and performance on the Brazelton Neonatal Behavioral Assessment Scale in a multiethnic pregnancy cohort. Am J Epidemiol. 2007;165:1397–404.CrossRef Engel SM, Berkowitz GS, Barr DB, Teitelbaum SL, Siskind J, Meisel SJ, et al. Prenatal organophosphate metabolite and organochlorine levels and performance on the Brazelton Neonatal Behavioral Assessment Scale in a multiethnic pregnancy cohort. Am J Epidemiol. 2007;165:1397–404.CrossRef
9.
go back to reference Lu C, Toepel K, Irish R, Fenske RA, Barr DB, Bravo R. Organic diets significantly lower children’s dietary exposure to organophosphorus pesticides. Environ Health Perspect. 2006;114:260–3.CrossRef Lu C, Toepel K, Irish R, Fenske RA, Barr DB, Bravo R. Organic diets significantly lower children’s dietary exposure to organophosphorus pesticides. Environ Health Perspect. 2006;114:260–3.CrossRef
10.
go back to reference Needham LL. Assessing exposure to organophosphorus pesticides by biomonitoring in epidemiologic studies of birth outcomes. Environ Health Perspect. 2005;113:494–8.CrossRef Needham LL. Assessing exposure to organophosphorus pesticides by biomonitoring in epidemiologic studies of birth outcomes. Environ Health Perspect. 2005;113:494–8.CrossRef
11.
go back to reference Barr DB. Biomonitoring of exposure to pesticides. J Chem Health Saf. 2008;15:20–9.CrossRef Barr DB. Biomonitoring of exposure to pesticides. J Chem Health Saf. 2008;15:20–9.CrossRef
12.
go back to reference Spaan S, Pronk A, Koch HM, Jusko TA, Jaddoe VW, Shaw PA, et al. Reliability of concentrations of organophosphate pesticide metabolites in serial urine specimens from pregnancy in the Generation R Study. J Expo Sci Environ Epidemiol. 2015;25:286–94.CrossRef Spaan S, Pronk A, Koch HM, Jusko TA, Jaddoe VW, Shaw PA, et al. Reliability of concentrations of organophosphate pesticide metabolites in serial urine specimens from pregnancy in the Generation R Study. J Expo Sci Environ Epidemiol. 2015;25:286–94.CrossRef
13.
go back to reference Lewis RC, Cantonwine DE, Anzalota Del Toro LV, Calafat AM, Valentin-Blasini L, Davis MD, et al. Distribution and determinants of urinary biomarkers of exposure to organophosphate insecticides in Puerto Rican pregnant women. Sci Total Environ. 2015;512-513:337–44.CrossRef Lewis RC, Cantonwine DE, Anzalota Del Toro LV, Calafat AM, Valentin-Blasini L, Davis MD, et al. Distribution and determinants of urinary biomarkers of exposure to organophosphate insecticides in Puerto Rican pregnant women. Sci Total Environ. 2015;512-513:337–44.CrossRef
14.
go back to reference Ueyama J, Saito I, Takaishi A, Nomura H, Inoue M, Osaka A, et al. A revised method for determination of dialkylphosphate levels in human urine by solid-phase extraction and liquid chromatography with tandem mass spectrometry: application to human urine samples from Japanese children. Environ Health Prev Med. 2014;19:405–13.CrossRef Ueyama J, Saito I, Takaishi A, Nomura H, Inoue M, Osaka A, et al. A revised method for determination of dialkylphosphate levels in human urine by solid-phase extraction and liquid chromatography with tandem mass spectrometry: application to human urine samples from Japanese children. Environ Health Prev Med. 2014;19:405–13.CrossRef
15.
go back to reference Oya N, Ito Y, Hioki K, Asai Y, Aoi A, Sugiura Y, et al. Quantitative analysis of organophosphate insecticide metabolites in urine extracted from disposable diapers of toddlers in Japan. Int J Hyg Environ Health. 2017;220:209–16.CrossRef Oya N, Ito Y, Hioki K, Asai Y, Aoi A, Sugiura Y, et al. Quantitative analysis of organophosphate insecticide metabolites in urine extracted from disposable diapers of toddlers in Japan. Int J Hyg Environ Health. 2017;220:209–16.CrossRef
16.
go back to reference Hornung RW, Reed LD. Estimation of average concentration in the presence of nondetectable values. Appl Occup Environ Hyg. 1990;5:46–51.CrossRef Hornung RW, Reed LD. Estimation of average concentration in the presence of nondetectable values. Appl Occup Environ Hyg. 1990;5:46–51.CrossRef
17.
go back to reference Fraselle S, De Cremer K, Coucke W, Glorieux G, Vanmassenhove J, Schepers E, et al. Development and validation of an ultra-high performance liquid chromatography-tandem mass spectrometry method to measure creatinine in human urine. J Chromatogr B Anal Technol Biomed Life Sci. 2015;988:88–97.CrossRef Fraselle S, De Cremer K, Coucke W, Glorieux G, Vanmassenhove J, Schepers E, et al. Development and validation of an ultra-high performance liquid chromatography-tandem mass spectrometry method to measure creatinine in human urine. J Chromatogr B Anal Technol Biomed Life Sci. 2015;988:88–97.CrossRef
18.
go back to reference Boeniger MF, Lowry LK, Rosenberg J. Interpretation of urine results used to assess chemical exposure with emphasis on creatinine adjustments: a review. Am Ind Hyg Assoc J. 1993;54(10):615–27.CrossRef Boeniger MF, Lowry LK, Rosenberg J. Interpretation of urine results used to assess chemical exposure with emphasis on creatinine adjustments: a review. Am Ind Hyg Assoc J. 1993;54(10):615–27.CrossRef
19.
go back to reference Koo TK, Li MY. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med. 2016;15:155–63.CrossRef Koo TK, Li MY. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med. 2016;15:155–63.CrossRef
20.
go back to reference Landis JR, Koch GG. An application of hierarchical kappa-type statistics in the assessment of majority agreement among multiple observers. Biometrics. 1977;33:363–74.CrossRef Landis JR, Koch GG. An application of hierarchical kappa-type statistics in the assessment of majority agreement among multiple observers. Biometrics. 1977;33:363–74.CrossRef
21.
go back to reference Lachin JM. The role of measurement reliability in clinical trials. Clin Trials. 2004;1:553–66.CrossRef Lachin JM. The role of measurement reliability in clinical trials. Clin Trials. 2004;1:553–66.CrossRef
22.
go back to reference Attfield KR, Hughes MD, Spengler JD, Lu C. Within- and between-child variation in repeated urinary pesticide metabolite measurements over a 1-year period. Environ Health Perspect. 2014;122:201–6.CrossRef Attfield KR, Hughes MD, Spengler JD, Lu C. Within- and between-child variation in repeated urinary pesticide metabolite measurements over a 1-year period. Environ Health Perspect. 2014;122:201–6.CrossRef
23.
go back to reference Garfitt SJ, Jones K, Mason HJ, Cocker J. Exposure to the organophosphate diazinon: data from a human volunteer study with oral and dermal doses. Toxicol Lett. 2002;134:105–13.CrossRef Garfitt SJ, Jones K, Mason HJ, Cocker J. Exposure to the organophosphate diazinon: data from a human volunteer study with oral and dermal doses. Toxicol Lett. 2002;134:105–13.CrossRef
24.
go back to reference Griffin P, Mason H, Heywood K, Cocker J. Oral and dermal absorption of chlorpyrifos: a human volunteer study. Occup Environ Med. 1999;56:10–3.CrossRef Griffin P, Mason H, Heywood K, Cocker J. Oral and dermal absorption of chlorpyrifos: a human volunteer study. Occup Environ Med. 1999;56:10–3.CrossRef
25.
go back to reference Ito Y, Ueyama J, Nakayama SF, Isobe T, Oya N, Sato H, et al. Within-individual and interlaboratory variability analyses of urinary metabolites measurements of organophosphorus insecticides. J Expo Sci Environ Epidemiol. in press. Ito Y, Ueyama J, Nakayama SF, Isobe T, Oya N, Sato H, et al. Within-individual and interlaboratory variability analyses of urinary metabolites measurements of organophosphorus insecticides. J Expo Sci Environ Epidemiol. in press.
26.
go back to reference Wielgomas B. Variability of urinary excretion of pyrethroid metabolites in seven persons over seven consecutive days—implications for observational studies. Toxicol Lett. 2013;221:15–22.CrossRef Wielgomas B. Variability of urinary excretion of pyrethroid metabolites in seven persons over seven consecutive days—implications for observational studies. Toxicol Lett. 2013;221:15–22.CrossRef
27.
go back to reference Rivera-Núñez Z, Meliker JR, Linder AM, Nriagu JO. Reliability of spot urine samples in assessing arsenic exposure. Int J Hyg Environ Health. 2010;213:259–64.CrossRef Rivera-Núñez Z, Meliker JR, Linder AM, Nriagu JO. Reliability of spot urine samples in assessing arsenic exposure. Int J Hyg Environ Health. 2010;213:259–64.CrossRef
Metadata
Title
Intra-individual variations of organophosphate pesticide metabolite concentrations in repeatedly collected urine samples from pregnant women in Japan
Authors
Keisuke Hioki
Yuki Ito
Naoko Oya
Shoji F. Nakayama
Tomohiko Isobe
Takeshi Ebara
Kanemitsu Shibata
Naomi Nishikawa
Kunihiko Nakai
Tomota Kamida
Jun Ueyama
Mayumi Sugiura-Ogasawara
Michihiro Kamijima
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Environmental Health and Preventive Medicine / Issue 1/2019
Print ISSN: 1342-078X
Electronic ISSN: 1347-4715
DOI
https://doi.org/10.1186/s12199-019-0761-4

Other articles of this Issue 1/2019

Environmental Health and Preventive Medicine 1/2019 Go to the issue