Combined effects of maternal exposure to fungicides on behavioral development in F


Journal

Birth defects research
ISSN: 2472-1727
Titre abrégé: Birth Defects Res
Pays: United States
ID NLM: 101701004

Informations de publication

Date de publication:
15 01 2020
Historique:
received: 04 06 2019
revised: 08 10 2019
accepted: 17 10 2019
pubmed: 5 11 2019
medline: 25 5 2021
entrez: 5 11 2019
Statut: ppublish

Résumé

Few published studies are reported for neurobehavioral toxicity of combined exposure to fungicides in mammals. This study was aimed to evaluate reproductive and neurobehavioral effects of maternal exposure to combined fungicides in mice. Imazalil (IMZ) and thiabendazole (TBZ) were given in the diet to provide levels of 0/0% (control), 0.0015/0.006% (IMZ/TBZ), 0.006/0.018%, and 0.024/0.054% during the gestation and lactation periods. Selected reproductive and neurobehavioral parameters were measured in the F No adverse effect of IMZ/TBZ was observed in litter size, litter weight, or sex ratio at birth. The average body weight of male and female offspring was increased significantly in treatment groups during the lactation period. With respect to behavioral developmental parameters, the swimming head angle on PND 7 of male offspring was significantly accelerated in the treatment groups. After weaning, the movement time of exploratory behavior shortened in a significant dose-related manner in adult males of the F The high-dose level of IMZ/TBZ in the present study produced several adverse effects in neurobehavioral parameters after weaning without concurrent chemical administration in mice.

Sections du résumé

BACKGROUND
Few published studies are reported for neurobehavioral toxicity of combined exposure to fungicides in mammals. This study was aimed to evaluate reproductive and neurobehavioral effects of maternal exposure to combined fungicides in mice.
METHODS
Imazalil (IMZ) and thiabendazole (TBZ) were given in the diet to provide levels of 0/0% (control), 0.0015/0.006% (IMZ/TBZ), 0.006/0.018%, and 0.024/0.054% during the gestation and lactation periods. Selected reproductive and neurobehavioral parameters were measured in the F
RESULTS
No adverse effect of IMZ/TBZ was observed in litter size, litter weight, or sex ratio at birth. The average body weight of male and female offspring was increased significantly in treatment groups during the lactation period. With respect to behavioral developmental parameters, the swimming head angle on PND 7 of male offspring was significantly accelerated in the treatment groups. After weaning, the movement time of exploratory behavior shortened in a significant dose-related manner in adult males of the F
CONCLUSIONS
The high-dose level of IMZ/TBZ in the present study produced several adverse effects in neurobehavioral parameters after weaning without concurrent chemical administration in mice.

Identifiants

pubmed: 31680484
doi: 10.1002/bdr2.1613
doi:

Substances chimiques

Fungicides, Industrial 0
Imidazoles 0
enilconazole 6K0NOF3XQ6
Thiabendazole N1Q45E87DT

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

141-161

Informations de copyright

© 2019 Wiley Periodicals, Inc.

Références

Abbey, H., & Howard, E. (1973). Statistical procedure in developmental studies on species with multiple offspring. Developmental Psychobiology, 6, 329-335.
Altman, J., & Sudarshan, K. (1975). Postnatal development of locomotion in the laboratory rat. Animal Behaviour, 23, 896-920.
Barlow, S. M., Knight, A. F., & Sullivan, F. M. (1978). Delay in postnatal growth and development of offspring produced by maternal restraint stress during pregnancy in the rat. Teratology, 18, 211-218.
Biel, W. C. (1940). Early age differences in maze performance in the albino rat. The Journal of Genetic Psychology, 56, 439-453.
Boobis, A. R., Ossendorp, B. C., Banasiak, U., Hamey, P. Y., Sebestyen, I., & Moretto, A. (2008). Cumulative risk assessment of pesticide residues in food. Toxicology Letters, 180, 137-150.
Crépet, A., Vanacker, M., Sprong, C., de Boer, W., Blaznik, U., Kennedy, M., … van Klaveren, J. (2019). Selecting mixtures on the basis of dietary exposure and hazard data: Application to pesticide exposure in the European population in relation to steatosis. International Journal of Hygiene and Environmental Health, 222, 291-306.
de Gavelle, E., de Lauzon-Guillain, B., Charles, M.-A., Chevrier, C., Hulin, M., Sirot, V., … Nougadère, A. (2016). Chronic dietary exposure to pesticide residues and associated risk in the French ELFE cohort of pregnant women. Environment International, 92-93, 533-542.
de Oliveira Neto, O. F., Arenas, A. Y., & Fostier, A. H. (2017). Sorption of thiabendazole in sub-tropical Brazilian soils. Environmental Science and Pollution Research, 26, 2421-2434.
European Food Safety Authority. (2010). Conclusion on pesticide peer review: Conclusion on the peer review of the pesticide risk assessment of the active substance imazalil. EFSA Journal, 8(3), 1-69.
European Food Safety Authority. (2014). Conclusion on pesticide peer review: Conclusion on the peer review of the pesticide risk assessment of the active substance thiabendazole. EFSA Journal, 12(11), 1-57.
Fox, W. M. (1965). Reflex-ontogeny and behavioural development of the mouse. Animal Behaviour, 13, 234-241.
Fujikoshi, Y. (2009). The mathematical principle of longitudinal analysis (series of statistical science of multivariate data, 6). Tokyo: Asakura Publishing (in Japanese).
Fujikoshi, Y., Kan, T., & Hijikata, Y. (2008). Applied longitudinal analysis. Tokyo: Ohmsha (in Japanese).
Fungicide Resistance Action Committee. (2018) FRAC Code List©*2018: Fungicides sorted by mode of action (including FRAC Code numbering). Retrieved from http://www.phi-base.org/images/fracCodeList.pdf.
Furusho, N., Otsuki, N., Ohtsuki, T., Tatebe-Sasaki, C., Sato, K., Akiyama, H., & Kawamura, Y. (2012). Improved methodology for quantitative determination of thiabendazole. Bulletin of National Institute of Health Science, 130, 46-49 (in Japanese).
Gioiosa, L., Fissore, E., Ghirardelli, G., Parmigiani, S., & Palanza, P. (2007). Developmental exposure to low-dose estrogenic endocrine disruptors alters sex differences in exploration and emotional responses in mice. Hormone and Behavior, 52, 307-316.
Gregory, E. H., & Pfaff, D. W. (1971). Development of olfactory-guided behavior in infant rats. Physiology & Behavior, 6, 573-576.
Hass, U., Boberg, J., Christiansen, S., Jacobsen, P. R., Vinggaard, A. M., Taxvig, C., … Axelstad, M. (2012). Adverse effects on sexual development in rat offspring after low dose exposure to a mixture of endocrine disrupting pesticides. Reproductive Toxicology, 34, 261-274.
Hass, U., Christiansen, S., Axelstad, M., Scholze, M., & Boberg, J. (2017). Combined exposure to low doses of pesticides causes decreased birth weights in rats. Reproductive Toxicology, 72, 97-105.
Iñigo-Nuñez, S., Herreros, M. A., Encinas, T., & Gonzalez-Bulnes, A. (2010). Estimated daily intake of pesticides and xenoestrogenic exposure by fruit consumption in the female population from a Mediterranean country (Spain). Food Control, 21, 471-477.
International Conference on Harmonization of Technical Requirement for Registration of Pharmaceuticals for Human Use. (2005). Detection of toxicity to reproduction for medicinal products & toxicity to male fertility. ICH Tripartite Guideline, S5(R2), 1-18.
Japan Plant Protection Association. (2005). Pesticide handbook [2005 edition] (pp. 326-327). Tokyo: Author (in Japanese).
Jin, Y., Zhu, Z., Wang, Y., Yang, E., Feng, X., & Fu, Z. (2016). The fungicide imazalil induces developmental abnormalities and alters locomotor activity during early developmental stages in zebrafish. Chemosphere, 153, 445-461.
Joint FAO/WHO Expert Committee on Food Additives. (1997). Food additives series 39: Toxicological evaluation of certain veterinary drug residues in food (pp. 3-9). Geneva: International Programme on Chemical Safety (IPCS).
Joint FAO/WHO Meeting on Pesticide Residues. (1977). Monographs of toxicological evaluations: 409. Imazalil (Pesticide residues in food: 1977 evaluations). International Programme on Chemical Safety (IPCS). Retrieved from http://www.inchem.org/documents/jmpr/jmpmono/v077pr31.htm
Joint FAO/WHO Meeting on Pesticide Residues. (1992). Pesticide residues in food - 1991. Evaluations 1991 part II - toxicology (pp. 283-285). Geneva: World Health Organization.
Joint FAO/WHO Meeting on Pesticide Residues. (2006). Pesticide residues in food - 2005. Evaluations 2005 part II - toxicological (pp. 303-314). Geneva: World Health Organization.
Joint FAO/WHO Meeting on Pesticide Residues. (2008). Pesticide residues in food - 2006. Evaluations 2006 part II - toxicological (pp. 429-450). Geneva: World Health Organization.
Kitatani, T., Akaike, M., Takayama, K., & Kobayashi, T. (1988). Teratological study of cefodizime sodium in mice. -intravenous administration during period of organogenesis. The Journal of Toxicological Sciences, 13(Suppl. I), 191-214 (in Japanese).
Lankas, G. R., & Wise, D. L. (1993). Developmental toxicity of orally administered thiabendazole in Sprague-Dawley rats and New Zealand white rabbits. Food and Chemical Toxicology, 31, 199-207.
Lankas, G. R., Nakatsuka, T., Ban, Y., Komatsu, T., & Matsumoto, H. (2001). Developmental toxicity of orally administered thiabendazole in ICR mice. Food and Chemical Toxicology, 39, 367-374.
Manabe, M., Kanda, S., Fukunaga, K., Tsubura, A., & Nishiyama, T. (2006). Evaluation of the estrogenic activities of some pesticides and their combinations using MtT/se cell proliferation assay. International Journal of Hygiene and Environmental Health., 209, 413-421.
Martin, P., & Bateson, P. (1990). Measuring behaviour: an introductory guide (pp. 102-122). Tokyo: Tokai University Press.
Meyer, O., & Hansen, E. (1980). Behavioural and developmental effects of butylated hydroxytoluene dosed rats in utero and in lactation period. Toxicology, 16, 247-258.
Mikami, Y., Toda, M., Watanabe, M., Nakamura, M., Toyama, Y., & Kawakami, Y. (2002). A simple and reliable behavioral analysis of locomotor function after spinal cord injury in mice. Journal of Neurosurgery, 97, 142-147.
Miyazaki, I., & Nakamura, H. (2006). Effects of antifungal paints and radiation of fungicides. Bulletin of Tokyo Metropolitan Industrial Technology Research Institute, 1, 114-115 (in Japanese).
Motz, B. A., & Alberts, J. R. (2005). The validity and utility of geotaxis in young rodents. Neurotoxicology and Teratology, 27, 529-533.
National Research Council. (2010). Guide for the care and use of laboratory animals (8th ed.). Washington D.C.: National Academies Press.
Nougadère, A., Sirot, V., Kadar, A., Fastier, A., Truchot, E., Vergnet, C., … Leblanc, J.-C. (2012). Total diet study on pesticide residues in France: Levels in food consumed and chronic dietary risk to consumers. Environment International, 45, 135-150.
Ogata, A., Ando, H., Kubo, Y., & Hiraga, K. (1984). Teratogenicity of thiabendazole in ICR mice. Food and Chemical Toxicology, 22, 509-520.
Ogawa, Y. (2018). The study of residues of agricultural chemicals-pesticides, veterinary drugs and feed additives in foods (2013-2015). Food Sanitation Research, 68(7), 7-23 (in Japanese).
Organization for Economic Cooperation and Development. (2007). Developmental neurotoxicity study. OECD Guideline for Testing Chemicals, 426, 1-26. Retrieved from http://titania.sourceoecd.org/vl=1469022/cl=13/nw=1/rpsv/cgi-bin/fulltextew.pl?prpsv=/ij/oecdjournals/1607310x/v1n4/s27/p1.idx
Orton, F., Rosivatz, E., Scholze, M., & Kortenkamp, A. (2011). Widely used pesticides with previously unknown endocrine activity revealed as in vitro antiandrogens. Environmental Health Perspectives, 119, 794-800.
Paget, G. E., & Thomson, R. (Eds.). (1979). Standard operating procedures in pathology (pp. 334-340). Tokyo: Seishin Shoin.
Palmer, A. K., & Ulbrich, B. C. (1997). The cult of culling. Fundamental and Applied Toxicology, 38, 7-22.
Pantaleoni, G., Fanini, D., Sponta, A. M., Palumbo, G., Giorgi, R., & Adams, P. M. (1988). Effects of maternal exposure to polychlorobiphenyls (PCBs) on F1 generation behavior in the rat. Fundamental and Applied Toxicology, 11, 440-449.
Picó, Y., El-Sheikh, M. A., Alfarhan, A. H., & Barceló, D. (2018). Target vs non-target analysis to determine pesticide residues in fruits from Saudi Arabia and influence in potential risk associated with exposure. Food and Chemical Toxicology, 111, 53-63.
Robinson, H. J., Phares, H. F., & Graessle, O. E. (1978). The toxicological and antifungal properties of thiabendazole. Ecotoxicology and Environmental Safety, 1, 471-476.
Schapiro, S., Salas, M., & Vukovich, K. (1970). Hormonal effects on ontogeny of swimming ability in the rat: Assessment of central nervous system development. Science, 168, 147-150.
Simpson, J., Ryan, C., Curley, A., Mulcaire, J., & Kelly, J. P. (2012). Sex differences in baseline and drug-induced behavioural responses in classical behavioural tests. Progress in Neuropsychopharmacology and Biological Psychiatry, 37, 227-236.
Şişman, T., & Türkez, H. (2010). Toxicologic evaluation of imazalil with particular reference to genotoxic and teratogenic potentials. Toxicology and Industrial Health, 26, 641-648.
Tanaka, T. (1995). Reproductive and neurobehavioral effects of imazalil administered to mice. Reproductive Toxicology, 9, 281-288.
Tanaka, T. (1998). Effects of litter size on behavioral development in mice. Reproductive Toxicology., 12, 613-617.
Tanaka, T. (2001). Reproductive and neurobehavioural effects of thiabendazole administered to mice in the diet. Food Additives and Contaminants, 18, 375-383.
Tanaka, T. (2004). The relationships between litter size, offspring weight, and behavioral development in laboratory mice Mus musculus. Mammal Study, 29, 147-153.
Tanaka, T. (2010). Biological factors influencing exploratory behavior in laboratory mice, Mus musculus. Mammal Study, 35, 139-144.
Tanaka, T. (2015a). Comparison of measurements of the same variables of exploratory behaviour in mice with different apparatuses. Journal of Experimental and Applied Animal Science, 1(3), 301-316.
Tanaka, T. (2015b). Sex differences in exploratory behaviour of laboratory CD-1 mice (Mus musculus). Scandinavian Journal of Laboratory Animal Science, 41(5), 1-9.
Tanaka, S., Kawashima, K., Nakaura, S., Takanaka, A., & Omori, Y. (1982). Effect of dietary administration of thiabendazole on pregnant rats and fetal development. Journal of the Food Hygienic Society of Japan, 23, 468-473.
Tanaka, T., Takahashi, O., & Oishi, S. (1992). Reproductive and neurobehavioural effects in three-generation toxicity study of piperonyl butoxide administered to mice. Food and Chemical Toxicology, 30, 1015-1019.
Tanaka, T., Takahashi, O., & Oishi, S. (1998). Developmental toxicity study of imazalil administered to mice in the diet. Annual Report of Tokyo Metropolitan Research Laboratory of Public Health, 49, 277-280 (in Japanese).
Tanaka, T., Ogata, A., Inomata, A., & Nakae, D. (2013). Effects of maternal exposure to imazalil on behavioral development in F1-generation mice. Birth Defects Research Part B: Developmental and Reproductive Toxicology, 98, 334-342.
The Japan Food Chemical Research Foundation. (2018a). Table of MRLs for Agricultural Chemicals: Imazalil. Retrieved from http://db.ffcr.or.jp/front/pesticide_detail?id=8500
The Japan Food Chemical Research Foundation. (2018b). Table of MRLs for Agricultural Chemicals: Thiabendazole. Retrieved from http://db.ffcr.or.jp/front/pesticide_detail?id=39500
The Ministry of Health, Labour and Welfare of Japan. (2017). The official inspection results of pesticide residues in food in fiscal year 2013-2014. Retrieved from http://www.mhlw.go.jp/file/06-Seisakujouhou-11130500-Shokuhinanzenbu/0000172509.pdf (in Japanese)
The Ministry of Health, Labour and Welfare of Japan. (2019). The official inspection results of daily intake of pesticide residues in food in fiscal year 2017. Retrieved from http://www.mhlw.go.jp/content/000495467.pdf (in Japanese)
The Science Council of Japan. (2006). Guidelines for proper conduct of animal experiments. The Science Council of Japan. Retrieved from http://www.scj.go.jp/ja/info/kohyo/pdf/kohyo-20-k16-2e.pdf
Thienpont, D., van Cutsem, J., van Cauteren, H., & Marsboom, R. (1981). The biological and toxicological properties of imazalil. Arzneimittel-Forschung/Drug Research, 31, 309-315.
Ujike, A., & Yasunaga, M. (2015). The residual situation of the fungicides in fruit processed foods. Annual Report of Kagawa Prefectural Research Institute for Environmental Sciences and Public Health, 14, 65-67 (in Japanese).
van Leemput, L., Swysen, E., Woestenborghs, R., Michielsen, L., Meuldermans, W., & Heykants, J. (1989). On the terrestrial toxicity of fungicide imazalil (enilconazole) to the earthworm species Eisenia foetida. Ecotoxicology and Environmental Safety, 18, 313-320.
Vorhees, C. V. (1986). Methods for assessing the adverse effects of foods and other chemicals on animal behavior. Nutrition Reviews, 44(Suppl), 185-193.
Vorhees, C. V., Brunner, R. L., & Butcher, R. E. (1979). Psychotropic drugs as behavioral teratogens. Science, 205, 1220-1225.
Weinstock, M. (2007). Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochemistry Research, 32, 1730-1740.
Wise, D. L., Cartwright, M. E., Seider, C. L., Sachuk, L. A., & Lankas, G. R. (1994). Dietary two-generation reproduction study of thiabendazole in Sprague-Dawley rats. Food and Chemical Toxicology, 32, 239-246.
Yoneyama, M., Ogata, A., Fujii, T., Mikuriya, H., Yano, N., Takahashi, H., … Hiraga, K. (1983). Absorption, distribution, excretion and placental transfer of thiabendazole in pregnant mice: Effect of two kinds of vehicle. Annual Report of the Tokyo Metropolitan Research Laboratory of Public Health, 34, 337-342 (in Japanese).
Yoneyama, M., Ogata, A., Fujii, T., & Hiraga, K. (1984). The maternal-foetal distribution of thiabendazole administered in two different vehicles to pregnant mice. Food and Chemical Toxicology, 22, 731-735.
Yoshimura, H., & Motomura, H. (2016). Survey of pesticide residues in agricultural products (2016). Annual Report of Nagasaki Prefectural Institute of Environment and Public Health, 62, 139-142 (in Japanese).

Auteurs

Toyohito Tanaka (T)

Division of Toxicology, Department of Pharmaceutical and Environmental Sciences, Tokyo Metropolitan Institute of Public Health, Tokyo, Japan.

Toshinari Suzuki (T)

Division of Toxicology, Department of Pharmaceutical and Environmental Sciences, Tokyo Metropolitan Institute of Public Health, Tokyo, Japan.

Akiko Inomata (A)

Department of Pharmaceutical and Environmental Sciences, Tokyo Metropolitan Institute of Public Health, Tokyo, Japan.

Takako Moriyasu (T)

Department of Pharmaceutical and Environmental Sciences, Tokyo Metropolitan Institute of Public Health, Tokyo, Japan.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH