Investigation of dichlorodiphenyltrichloroethane (DDT) on xenobiotic enzyme disruption and metabolomic bile acid biosynthesis in DDT-sprayed areas using wild rats

Dichlorodiphenyltrichloroethane (DDT) is an organochlorine insecticide used worldwide. Several studies have reported the toxic effects of DDT and its metabolites on steroid hormone biosynthesis; however, its environmental effects are not well understood. This study examined wild rats collected in DD...

Full description

Saved in:
Bibliographic Details
Published inJournal of Veterinary Medical Science Vol. 85; no. 2; pp. 236 - 243
Main Authors SMIT, Nico J, WEPENER, Victor, YOHANNES, Yared Beyene, NAKAYAMA, Shouta MM, ISHIZUKA, Mayumi, MOTOHIRA, Kodai, EGUCHI, Akifumi, VUREN, Johan HJ VAN, IKENAKA, Yoshinori
Format Journal Article
LanguageEnglish
Published Japan JAPANESE SOCIETY OF VETERINARY SCIENCE 2023
Japan Science and Technology Agency
The Japanese Society of Veterinary Science
Subjects
Online AccessGet full text
ISSN0916-7250
1347-7439
1347-7439
DOI10.1292/jvms.22-0490

Cover

Loading…
Abstract Dichlorodiphenyltrichloroethane (DDT) is an organochlorine insecticide used worldwide. Several studies have reported the toxic effects of DDT and its metabolites on steroid hormone biosynthesis; however, its environmental effects are not well understood. This study examined wild rats collected in DDT-sprayed areas of South Africa and quantified plasma metabolites using liquid chromatography quadrupole time-of-flight mass spectrometry (LC-Q-TOF-MS). Fold change analysis of the metabolome revealed the effect of DDT on bile acid biosynthesis. Gene expression of the related enzyme in rat liver samples was also quantified. Significant association was found between DDT and gene expression levels related to constitutive androstane receptor mediated enzymes, such as Cyp2b1 in rat livers. However, our results could not fully demonstrate that enzymes related to bile acid biosynthesis were strongly affected by DDT. The correlation between DDT concentration and gene expression involved in steroid hormone synthesis in testis was also evaluated; however, no significant correlation was found. The disturbance of metabolic enzymes occurred in rat liver in the target area. Our results suggest that DDT exposure affects gene expression in wild rats living in DDT-sprayed areas. Therefore, there is a need for DDT toxicity evaluation in mammals living in DDT-sprayed areas. We could not find an effective biomarker that could reflect the mechanism of DDT exposure; however, this approach can provide new insights for future research to evaluate DDT effects in sprayed areas.
AbstractList Dichlorodiphenyltrichloroethane (DDT) is an organochlorine insecticide used worldwide. Several studies have reported the toxic effects of DDT and its metabolites on steroid hormone biosynthesis; however, its environmental effects are not well understood. This study examined wild rats collected in DDT-sprayed areas of South Africa and quantified plasma metabolites using liquid chromatography quadrupole time-of-flight mass spectrometry (LC-Q-TOF-MS). Fold change analysis of the metabolome revealed the effect of DDT on bile acid biosynthesis. Gene expression of the related enzyme in rat liver samples was also quantified. Significant association was found between DDT and gene expression levels related to constitutive androstane receptor mediated enzymes, such as Cyp2b1 in rat livers. However, our results could not fully demonstrate that enzymes related to bile acid biosynthesis were strongly affected by DDT. The correlation between DDT concentration and gene expression involved in steroid hormone synthesis in testis was also evaluated; however, no significant correlation was found. The disturbance of metabolic enzymes occurred in rat liver in the target area. Our results suggest that DDT exposure affects gene expression in wild rats living in DDT-sprayed areas. Therefore, there is a need for DDT toxicity evaluation in mammals living in DDT-sprayed areas. We could not find an effective biomarker that could reflect the mechanism of DDT exposure; however, this approach can provide new insights for future research to evaluate DDT effects in sprayed areas.
Dichlorodiphenyltrichloroethane (DDT) is an organochlorine insecticide used worldwide. Several studies have reported the toxic effects of DDT and its metabolites on steroid hormone biosynthesis; however, its environmental effects are not well understood. This study examined wild rats collected in DDT-sprayed areas of South Africa and quantified plasma metabolites using liquid chromatography quadrupole time-of-flight mass spectrometry (LC-Q-TOF-MS). Fold change analysis of the metabolome revealed the effect of DDT on bile acid biosynthesis. Gene expression of the related enzyme in rat liver samples was also quantified. Significant association was found between DDT and gene expression levels related to constitutive androstane receptor mediated enzymes, such as Cyp2b1 in rat livers. However, our results could not fully demonstrate that enzymes related to bile acid biosynthesis were strongly affected by DDT. The correlation between DDT concentration and gene expression involved in steroid hormone synthesis in testis was also evaluated; however, no significant correlation was found. The disturbance of metabolic enzymes occurred in rat liver in the target area. Our results suggest that DDT exposure affects gene expression in wild rats living in DDT-sprayed areas. Therefore, there is a need for DDT toxicity evaluation in mammals living in DDT-sprayed areas. We could not find an effective biomarker that could reflect the mechanism of DDT exposure; however, this approach can provide new insights for future research to evaluate DDT effects in sprayed areas.Dichlorodiphenyltrichloroethane (DDT) is an organochlorine insecticide used worldwide. Several studies have reported the toxic effects of DDT and its metabolites on steroid hormone biosynthesis; however, its environmental effects are not well understood. This study examined wild rats collected in DDT-sprayed areas of South Africa and quantified plasma metabolites using liquid chromatography quadrupole time-of-flight mass spectrometry (LC-Q-TOF-MS). Fold change analysis of the metabolome revealed the effect of DDT on bile acid biosynthesis. Gene expression of the related enzyme in rat liver samples was also quantified. Significant association was found between DDT and gene expression levels related to constitutive androstane receptor mediated enzymes, such as Cyp2b1 in rat livers. However, our results could not fully demonstrate that enzymes related to bile acid biosynthesis were strongly affected by DDT. The correlation between DDT concentration and gene expression involved in steroid hormone synthesis in testis was also evaluated; however, no significant correlation was found. The disturbance of metabolic enzymes occurred in rat liver in the target area. Our results suggest that DDT exposure affects gene expression in wild rats living in DDT-sprayed areas. Therefore, there is a need for DDT toxicity evaluation in mammals living in DDT-sprayed areas. We could not find an effective biomarker that could reflect the mechanism of DDT exposure; however, this approach can provide new insights for future research to evaluate DDT effects in sprayed areas.
Dichlorodiphenyltrichloroethane (DDT) is an organochlorine insecticide used worldwide. Several studies have reported the toxic effects of DDT and its metabolites on steroid hormone biosynthesis; however, its environmental effects are not well understood. This study examined wild rats collected in DDT-sprayed areas of South Africa and quantified plasma metabolites using liquid chromatography quadrupole time-of-flight mass spectrometry (LC-Q-TOF-MS). Fold change analysis of the metabolome revealed the effect of DDT on bile acid biosynthesis. Gene expression of the related enzyme in rat liver samples was also quantified. Significant association was found between DDT and gene expression levels related to constitutive androstane receptor mediated enzymes, such as Cyp2b1 in rat livers. However, our results could not fully demonstrate that enzymes related to bile acid biosynthesis were strongly affected by DDT. The correlation between DDT concentration and gene expression involved in steroid hormone synthesis in testis was also evaluated; however, no significant correlation was found. The disturbance of metabolic enzymes occurred in rat liver in the target area. Our results suggest that DDT exposure affects gene expression in wild rats living in DDT-sprayed areas. Therefore, there is a need for DDT toxicity evaluation in mammals living in DDT-sprayed areas. We could not find an effective biomarker that could reflect the mechanism of DDT exposure; however, this approach can provide new insights for future research to evaluate DDT effects in sprayed areas.
ArticleNumber 22-0490
Author EGUCHI, Akifumi
WEPENER, Victor
NAKAYAMA, Shouta MM
VUREN, Johan HJ VAN
IKENAKA, Yoshinori
SMIT, Nico J
MOTOHIRA, Kodai
YOHANNES, Yared Beyene
ISHIZUKA, Mayumi
Author_xml – sequence: 1
  fullname: SMIT, Nico J
  organization: Water Research Group, Unit for Environmental Sciences and Management, Potchefstroom Campus, North-West University, Potchefstroom, South Africa
– sequence: 1
  fullname: WEPENER, Victor
  organization: Water Research Group, Unit for Environmental Sciences and Management, Potchefstroom Campus, North-West University, Potchefstroom, South Africa
– sequence: 1
  fullname: YOHANNES, Yared Beyene
  organization: Department of Chemistry, College of Natural and Computational Science, University of Gondar, Gondar, Ethiopia
– sequence: 1
  fullname: NAKAYAMA, Shouta MM
  organization: Biomedical Sciences Department, School of Veterinary Medicine, The University of Zambia, Lusaka, Zambia
– sequence: 1
  fullname: ISHIZUKA, Mayumi
  organization: Laboratory of Toxicology, Department of Environmental Veterinary Sciences, Laboratory of Toxicology, Hokkaido University, Hokkaido, Japan
– sequence: 1
  fullname: MOTOHIRA, Kodai
  organization: Laboratory of Toxicology, Department of Environmental Veterinary Sciences, Laboratory of Toxicology, Hokkaido University, Hokkaido, Japan
– sequence: 1
  fullname: EGUCHI, Akifumi
  organization: Center for Preventive Medical Sciences, Chiba University, Chiba, Japan
– sequence: 1
  fullname: VUREN, Johan HJ VAN
  organization: Water Research Group, Unit for Environmental Sciences and Management, Potchefstroom Campus, North-West University, Potchefstroom, South Africa
– sequence: 1
  fullname: IKENAKA, Yoshinori
  organization: One Health Research Center, Hokkaido University, Hokkaido, Japan
BackLink https://www.ncbi.nlm.nih.gov/pubmed/36596564$$D View this record in MEDLINE/PubMed
BookMark eNp1kk1vEzEQhleoiKaFG2dkiUuR2GJ7d-34VEHLR6VKXMrZcryzWUdeO9jeQPg5_FKcbBpBJS62NfPMq9czc1acOO-gKF4SfEmooO9WmyFeUlriWuAnxYxUNS95XYmTYoYFYSWnDT4tzmJcYUxJzcSz4rRijWANq2fF71u3gZjMUiXjHfIdao3urQ--Nese3NamcAhA6pUDdHFzc_8GZfYnOL8wPhmNwP3aDpBLYxjXeyHlWjRAUgtv_ZCJhbGAlDZtfvm4damHaCIyDmW5Mq6D2kKLVAAV0RiNW6IfxrYoqBSfF087ZSO8ONznxbdPH--vv5R3Xz_fXr-_KzVjJJWc1Q3jQlWcKdaRTrGGNE2NuwoDYS0X81qLdkEqNcdEMN1pIRjhdatFRWmOnxdXk-56XAzQanApKCvXwQwqbKVXRv6bcaaXS7-RBGPC8yiywsVBIfjvY26rHEzUYG3umx-jpJzhOeENrTL6-hG68mNw-X-ZmjNOM7kTfPW3paOXh_llgE6ADj7GAJ3UJu1HmR0am63J3ZLI3ZJISuVuSXLR20dFD7r_wT9M-ComtYQjrEIevYUJnjeS7o-p6JjUvQoSXPUHM_7aBg
CitedBy_id crossref_primary_10_1016_j_ecoenv_2024_116001
crossref_primary_10_1016_j_etap_2024_104514
crossref_primary_10_1016_j_ntt_2024_107323
crossref_primary_10_1007_s10653_024_02282_y
Cites_doi 10.1016/j.envint.2017.12.039
10.3389/fendo.2019.00886
10.1002/hep.20784
10.14573/altex.2013.2.209
10.1021/acs.jafc.7b00292
10.2133/dmpk.23.196
10.1016/j.tox.2016.11.016
10.1021/es5002105
10.1292/jvms.19-0168
10.1016/S0140-6736(05)67182-6
10.1093/toxsci/kfl051
10.1007/s11306-010-0231-x
10.1016/j.taap.2006.02.015
10.1016/j.mce.2019.02.016
10.1038/375581a0
10.1016/S0006-2952(00)00281-1
10.1016/j.envint.2015.12.015
10.1124/dmd.108.024190
10.1002/jssc.200700601
10.1371/journal.pone.0103337
10.1016/j.tox.2011.01.007
10.1292/jvms.09-0397
10.1186/s12958-017-0259-0
10.1016/j.envint.2017.02.011
10.1289/ehp.1002616
10.1016/j.bbalip.2009.01.016
10.1152/ajpgi.00357.2007
10.1007/s10552-017-0854-6
10.1111/j.1742-7843.2009.00439.x
10.1007/s11357-020-00188-y
10.5487/TR.2016.32.1.021
10.12703/b/9-7
10.1248/bpb.34.1116
10.1016/j.reprotox.2019.05.059
10.1093/toxsci/kfp130
10.1289/EHP2129
10.1016/j.taap.2013.05.008
10.1016/j.toxlet.2011.08.013
10.1007/BF01686072
10.1074/jbc.R112.431916
10.7717/peerj.143
10.1111/j.2517-6161.1995.tb02031.x
10.1016/j.chemosphere.2021.131815
10.1016/j.chemosphere.2015.08.029
10.1038/s41598-020-61767-9
10.1002/hep.21528
10.1016/j.etap.2018.02.004
10.1016/j.cbpc.2021.109173
10.1016/j.bbamcr.2006.09.001
10.1146/annurev.biochem.72.121801.161712
ContentType Journal Article
Copyright 2023 by the Japanese Society of Veterinary Science
2023. This work is published under https://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2023 The Japanese Society of Veterinary Science 2023
Copyright_xml – notice: 2023 by the Japanese Society of Veterinary Science
– notice: 2023. This work is published under https://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: 2023 The Japanese Society of Veterinary Science 2023
DBID AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
7QR
7U9
8FD
FR3
H94
M7N
P64
7X8
5PM
DOI 10.1292/jvms.22-0490
DatabaseName CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
Chemoreception Abstracts
Virology and AIDS Abstracts
Technology Research Database
Engineering Research Database
AIDS and Cancer Research Abstracts
Algology Mycology and Protozoology Abstracts (Microbiology C)
Biotechnology and BioEngineering Abstracts
MEDLINE - Academic
PubMed Central (Full Participant titles)
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
Virology and AIDS Abstracts
Technology Research Database
Algology Mycology and Protozoology Abstracts (Microbiology C)
AIDS and Cancer Research Abstracts
Chemoreception Abstracts
Engineering Research Database
Biotechnology and BioEngineering Abstracts
MEDLINE - Academic
DatabaseTitleList Virology and AIDS Abstracts

MEDLINE - Academic

MEDLINE
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
DeliveryMethod fulltext_linktorsrc
Discipline Veterinary Medicine
EISSN 1347-7439
EndPage 243
ExternalDocumentID PMC10017292
36596564
10_1292_jvms_22_0490
article_jvms_85_2_85_22_0490_article_char_en
Genre Journal Article
GroupedDBID 29L
2WC
53G
5GY
ACGFO
ACIWK
ACPRK
ADBBV
ADRAZ
AENEX
AFRAH
AI.
ALMA_UNASSIGNED_HOLDINGS
AOIJS
B.T
BAWUL
CS3
DIK
DU5
E3Z
EBS
ECGQY
EJD
EYRJQ
HYE
JSF
JSH
KQ8
M48
N5S
OK1
OVT
P2P
PGMZT
RJT
RNS
RPM
RZJ
TKC
TR2
VH1
XSB
AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
M~E
NPM
7QR
7U9
8FD
FR3
H94
M7N
P64
7X8
5PM
ID FETCH-LOGICAL-c661t-7645679a376a6f1fa6515540f30e16d7984c9db13a80196cfc996174dc9322b13
IEDL.DBID M48
ISSN 0916-7250
1347-7439
IngestDate Thu Aug 21 18:37:31 EDT 2025
Fri Jul 11 00:45:48 EDT 2025
Mon Jun 30 06:22:39 EDT 2025
Thu Jan 02 22:54:09 EST 2025
Tue Jul 01 00:31:11 EDT 2025
Thu Apr 24 22:59:40 EDT 2025
Wed Sep 03 06:31:12 EDT 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 2
Keywords wild rat
bile acid biosynthesis
steroid hormone biosynthesis
dichlorodiphenyltrichloroethane (DDT)
metabolomics
Language English
License https://creativecommons.org/licenses/by-nc-nd/4.0
This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial No Derivatives (by-nc-nd) License. (CC-BY-NC-ND 4.0: https://creativecommons.org/licenses/by-nc-nd/4.0/)
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c661t-7645679a376a6f1fa6515540f30e16d7984c9db13a80196cfc996174dc9322b13
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
content type line 23
OpenAccessLink http://journals.scholarsportal.info/openUrl.xqy?doi=10.1292/jvms.22-0490
PMID 36596564
PQID 2786726082
PQPubID 2028964
PageCount 8
ParticipantIDs pubmedcentral_primary_oai_pubmedcentral_nih_gov_10017292
proquest_miscellaneous_2760817523
proquest_journals_2786726082
pubmed_primary_36596564
crossref_citationtrail_10_1292_jvms_22_0490
crossref_primary_10_1292_jvms_22_0490
jstage_primary_article_jvms_85_2_85_22_0490_article_char_en
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 2023-00-00
PublicationDateYYYYMMDD 2023-01-01
PublicationDate_xml – year: 2023
  text: 2023-00-00
PublicationDecade 2020
PublicationPlace Japan
PublicationPlace_xml – name: Japan
– name: Tokyo
PublicationTitle Journal of Veterinary Medical Science
PublicationTitleAlternate J. Vet. Med. Sci.
PublicationYear 2023
Publisher JAPANESE SOCIETY OF VETERINARY SCIENCE
Japan Science and Technology Agency
The Japanese Society of Veterinary Science
Publisher_xml – name: JAPANESE SOCIETY OF VETERINARY SCIENCE
– name: Japan Science and Technology Agency
– name: The Japanese Society of Veterinary Science
References 25. Marouani N, Hallegue D, Sakly M, Benkhalifa M, ben Rhouma K, Tebourbi O. 2017. p,p’-DDT induces testicular oxidative stress-induced apoptosis in adult rats. Reprod Biol Endocrinol 15: 40.
3. Asaoka Y, Sakai H, Sasaki J, Goryo M, Yanai T, Masegi T, Okada K. 2010. Changes in the gene expression and enzyme activity of hepatic cytochrome P450 in juvenile Sprague-Dawley rats. J Vet Med Sci 72: 471–479.
18. Kelce WR, Stone CR, Laws SC, Gray LE, Kemppainen JA, Wilson EM. 1995. Persistent DDT metabolite p,p′-DDE is a potent androgen receptor antagonist. Nature 375: 581–585.
5. Bornman M, Delport R, Farías P, Aneck-Hahn N, Patrick S, Millar RP, de Jager C. 2018. Alterations in male reproductive hormones in relation to environmental DDT exposure. Environ Int 113: 281–289.
19. Krause W. 1977. Influence of DDT, DDVP and malathion on FSH, LH and testosterone serum levels and testosterone concentration in testis. Bull Environ Contam Toxicol 18: 231–242.
11. Govere JM, Durrheim DN, Kunene S. 2002. Malaria trends in South Africa and Swaziland and the introduction of synthetic pyrethroids to replace DDT for malaria vector control. S Afr J Sci 98: 19–21.
51. Zhu QN, Xie HM, Zhang D, Liu J, Lu YF. 2013. Hepatic bile acids and bile acid-related gene expression in pregnant and lactating rats. PeerJ 1: e143.
24. Liu L, Wu Q, Miao X, Fan T, Meng Z, Chen X, Zhu W. 2022. Study on toxicity effects of environmental pollutants based on metabolomics: A review. Chemosphere 286: 131815.
26. Mellert W, Kapp M, Strauss V, Wiemer J, Kamp H, Walk T, Looser R, Prokoudine A, Fabian E, Krennrich G, Herold M, van Ravenzwaay B. 2011. Nutritional impact on the plasma metabolome of rats. Toxicol Lett 207: 173–181.
16. Kawase A, Fujii A, Negoro M, Akai R, Ishikubo M, Komura H, Iwaki M. 2008. Differences in cytochrome P450 and nuclear receptor mRNA levels in liver and small intestines between SD and DA rats. Drug Metab Pharmacokinet 23: 196–206.
47. Wolmarans NJ, Bervoets L, Meire P, Wepener V. 2022. Sub-lethal exposure to malaria vector control pesticides causes alterations in liver metabolomics and behaviour of the African clawed frog (Xenopus laevis). Comp Biochem Physiol C Toxicol Pharmacol 251: 109173.
48. Yanagiba Y, Ito Y, Kamijima M, Gonzalez FJ, Nakajima T. 2009. Octachlorostyrene induces cytochrome P450, UDP-glucuronosyltransferase, and sulfotransferase via the aryl hydrocarbon receptor and constitutive androstane receptor. Toxicol Sci 111: 19–26.
21. Lee KJ, Wui SU, Heo J, Kim SH, Jeong JY, Lee JB. 2003. DDT reduced testosterone and aromatase activity via ER receptor in leydig cell. Environ Anal Health Toxicol 18: 95–100.
42. VoPham T, Bertrand KA, Hart JE, Laden F, Brooks MM, Yuan JM, Talbott EO, Ruddell D, Chang CH, Weissfeld JL. 2017. Pesticide exposure and liver cancer: a review. Cancer Causes Control 28: 177–190.
28. Miksys S, Hoffmann E, Tyndale RF. 2000. Regional and cellular induction of nicotine-metabolizing CYP2B1 in rat brain by chronic nicotine treatment. Biochem Pharmacol 59: 1501–1511.
38. Sanderson JT. 2006. The steroid hormone biosynthesis pathway as a target for endocrine-disrupting chemicals. Toxicol Sci 94: 3–21.
36. Safe S. 2020. Recent advances in understanding endocrine disruptors: DDT and related compounds. Fac Rev 9: 7.
41. Tully DB, Bao W, Goetz AK, Blystone CR, Ren H, Schmid JE, Strader LF, Wood CR, Best DS, Narotsky MG, Wolf DC, Rockett JC, Dix DJ. 2006. Gene expression profiling in liver and testis of rats to characterize the toxicity of triazole fungicides. Toxicol Appl Pharmacol 215: 260–273.
1. Aliferis KA, Chrysayi-Tokousbalides M. 2011. Metabolomics in pesticide research and development: review and future perspectives. Metabolomics 7: 35–53.
14. Issaq HJ, Abbott E, Veenstra TD. 2008. Utility of separation science in metabolomic studies. J Sep Sci 31: 1936–1947.
39. Schymanski EL, Jeon J, Gulde R, Fenner K, Ruff M, Singer HP, Hollender J. 2014. Identifying small molecules via high resolution mass spectrometry: communicating confidence. Environ Sci Technol 48: 2097–2098.
46. Wojciechowska A, Mlynarczuk J, Kotwica J. 2017. Changes in the mRNA expression of structural proteins, hormone synthesis and secretion from bovine placentome sections after DDT and DDE treatment. Toxicology 375: 1–9.
27. Michihara A, Anraku M, Abe A, Kinoshita H, Kamizaki Y, Tomida H, Akasaki K. 2011. Comparison of receptors and enzymes regulating cholesterol levels in liver between SHR/NDmcr-cp rats and normotensive Wistar Kyoto rats at ten weeks of age. Biol Pharm Bull 34: 1116–1119.
37. Salihovic S, Ganna A, Fall T, Broeckling CD, Prenni JE, van Bavel B, Lind PM, Ingelsson E, Lind L. 2016. The metabolic fingerprint of p,p′-DDE and HCB exposure in humans. Environ Int 88: 60–66.
31. Petersson J, Schreiber O, Steege A, Patzak A, Hellsten A, Phillipson M, Holm L. 2007. eNOS involved in colitis-induced mucosal blood flow increase. Am J Physiol Gastrointest Liver Physiol 293: G1281–G1287.
49. Yi M, Fashe M, Arakawa S, Moore R, Sueyoshi T, Negishi M. 2020. Nuclear receptor CAR-ERα signaling regulates the estrogen sulfotransferase gene in the liver. Sci Rep 10: 5001.
34. Rogan WJ, Chen A. 2005. Health risks and benefits of bis(4-chlorophenyl)-1,1,1-trichloroethane (DDT). Lancet 366: 763–773.
22. Liaset B, Madsen L, Hao Q, Criales G, Mellgren G, Marschall HU, Hallenborg P, Espe M, Frøyland L, Kristiansen K. 2009. Fish protein hydrolysate elevates plasma bile acids and reduces visceral adipose tissue mass in rats. Biochim Biophys Acta 1791: 254–262.
32. Pikuleva IA, Waterman MR. 2013. Cytochromes p450: roles in diseases. J Biol Chem 288: 17091–17098.
52. Zhu Q, Dong Y, Li X, Ni C, Huang T, Sun J, Ge RS. 2020. Dehydroepiandrosterone and Its CYP7B1 metabolite 7α-hydroxydehydroepiandrosterone regulates 11β-hydroxysteroid dehydrogenase 1 directions in rat leydig cells. Front Endocrinol (Lausanne) 10: 886.
45. Williams GP, Darbre PD. 2019. Low-dose environmental endocrine disruptors, increase aromatase activity, estradiol biosynthesis and cell proliferation in human breast cells. Mol Cell Endocrinol 486: 55–64.
43. Wagner M, Halilbasic E, Marschall HU, Zollner G, Fickert P, Langner C, Zatloukal K, Denk H, Trauner M. 2005. CAR and PXR agonists stimulate hepatic bile acid and bilirubin detoxification and elimination pathways in mice. Hepatology 42: 420–430.
6. Buckley DB, Klaassen
44
45
46
47
48
49
50
51
52
10
11
12
13
14
15
16
17
18
19
1
2
3
4
5
6
7
8
9
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
References_xml – reference: 29. Motohira K, Ikenaka Y, Yohannes YB, Nakayama SMM, Wepener V, Smit NJ, VAN Vuren JHJ, Sousa AC, Enuneku AA, Ogbomida ET, Ishizuka M. 2019. Dichlorodiphenyltrichloroethane (DDT) levels in rat livers collected from a malaria vector control region. J Vet Med Sci 81: 1575–1579.
– reference: 4. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate-a practical and powerful approach to multiple testing. J R Stat Soc B 57: 289–300.
– reference: 15. Jellali R, Zeller P, Gilard F, Legendre A, Fleury MJ, Jacques S, Tcherkez G, Leclerc E. 2018. Effects of DDT and permethrin on rat hepatocytes cultivated in microfluidic biochips: Metabolomics and gene expression study. Environ Toxicol Pharmacol 59: 1–12.
– reference: 8. Eguchi A, Sakurai K, Watanabe M, Mori C. 2017. Exploration of potential biomarkers and related biological pathways for PCB exposure in maternal and cord serum: a pilot birth cohort study in Chiba, Japan. Environ Int 102: 157–164.
– reference: 24. Liu L, Wu Q, Miao X, Fan T, Meng Z, Chen X, Zhu W. 2022. Study on toxicity effects of environmental pollutants based on metabolomics: A review. Chemosphere 286: 131815.
– reference: 38. Sanderson JT. 2006. The steroid hormone biosynthesis pathway as a target for endocrine-disrupting chemicals. Toxicol Sci 94: 3–21.
– reference: 14. Issaq HJ, Abbott E, Veenstra TD. 2008. Utility of separation science in metabolomic studies. J Sep Sci 31: 1936–1947.
– reference: 18. Kelce WR, Stone CR, Laws SC, Gray LE, Kemppainen JA, Wilson EM. 1995. Persistent DDT metabolite p,p′-DDE is a potent androgen receptor antagonist. Nature 375: 581–585.
– reference: 47. Wolmarans NJ, Bervoets L, Meire P, Wepener V. 2022. Sub-lethal exposure to malaria vector control pesticides causes alterations in liver metabolomics and behaviour of the African clawed frog (Xenopus laevis). Comp Biochem Physiol C Toxicol Pharmacol 251: 109173.
– reference: 9. Eskenazi B, An S, Rauch SA, Coker ES, Maphula A, Obida M, Crause M, Kogut KR, Bornman R, Chevrier J. 2018. Prenatal exposure to DDT and pyrethroids for malaria control and child neurodevelopment: The VHEMBE cohort, South Africa. Environ Health Perspect 126: 047004–1–047004–11.
– reference: 17. Kazantseva YA, Yarushkin AA, Pustylnyak VO. 2013. Dichlorodiphenyltrichloroethane technical mixture regulates cell cycle and apoptosis genes through the activation of CAR and ERα in mouse livers. Toxicol Appl Pharmacol 271: 137–143.
– reference: 28. Miksys S, Hoffmann E, Tyndale RF. 2000. Regional and cellular induction of nicotine-metabolizing CYP2B1 in rat brain by chronic nicotine treatment. Biochem Pharmacol 59: 1501–1511.
– reference: 40. Song Q, Chen H, Li Y, Zhou H, Han Q, Diao X. 2016. Toxicological effects of benzo(a)pyrene, DDT and their mixture on the green mussel Perna viridis revealed by proteomic and metabolomic approaches. Chemosphere 144: 214–224.
– reference: 1. Aliferis KA, Chrysayi-Tokousbalides M. 2011. Metabolomics in pesticide research and development: review and future perspectives. Metabolomics 7: 35–53.
– reference: 22. Liaset B, Madsen L, Hao Q, Criales G, Mellgren G, Marschall HU, Hallenborg P, Espe M, Frøyland L, Kristiansen K. 2009. Fish protein hydrolysate elevates plasma bile acids and reduces visceral adipose tissue mass in rats. Biochim Biophys Acta 1791: 254–262.
– reference: 3. Asaoka Y, Sakai H, Sasaki J, Goryo M, Yanai T, Masegi T, Okada K. 2010. Changes in the gene expression and enzyme activity of hepatic cytochrome P450 in juvenile Sprague-Dawley rats. J Vet Med Sci 72: 471–479.
– reference: 46. Wojciechowska A, Mlynarczuk J, Kotwica J. 2017. Changes in the mRNA expression of structural proteins, hormone synthesis and secretion from bovine placentome sections after DDT and DDE treatment. Toxicology 375: 1–9.
– reference: 41. Tully DB, Bao W, Goetz AK, Blystone CR, Ren H, Schmid JE, Strader LF, Wood CR, Best DS, Narotsky MG, Wolf DC, Rockett JC, Dix DJ. 2006. Gene expression profiling in liver and testis of rats to characterize the toxicity of triazole fungicides. Toxicol Appl Pharmacol 215: 260–273.
– reference: 42. VoPham T, Bertrand KA, Hart JE, Laden F, Brooks MM, Yuan JM, Talbott EO, Ruddell D, Chang CH, Weissfeld JL. 2017. Pesticide exposure and liver cancer: a review. Cancer Causes Control 28: 177–190.
– reference: 49. Yi M, Fashe M, Arakawa S, Moore R, Sueyoshi T, Negishi M. 2020. Nuclear receptor CAR-ERα signaling regulates the estrogen sulfotransferase gene in the liver. Sci Rep 10: 5001.
– reference: 2. Alsiö J, Birgner C, Björkblom L, Isaksson P, Bergström L, Schiöth HB, Lindblom J. 2009. Impact of nandrolone decanoate on gene expression in endocrine systems related to the adverse effects of anabolic androgenic steroids. Basic Clin Pharmacol Toxicol 105: 307–314.
– reference: 5. Bornman M, Delport R, Farías P, Aneck-Hahn N, Patrick S, Millar RP, de Jager C. 2018. Alterations in male reproductive hormones in relation to environmental DDT exposure. Environ Int 113: 281–289.
– reference: 52. Zhu Q, Dong Y, Li X, Ni C, Huang T, Sun J, Ge RS. 2020. Dehydroepiandrosterone and Its CYP7B1 metabolite 7α-hydroxydehydroepiandrosterone regulates 11β-hydroxysteroid dehydrogenase 1 directions in rat leydig cells. Front Endocrinol (Lausanne) 10: 886.
– reference: 44. Wang D, Zhu W, Wang Y, Yan J, Teng M, Miao J, Zhou Z. 2017. Metabolomics approach to investigate estrogen receptor-dependent and independent effects of o,p′-DDT in the uterus and brain of immature mice. J Agric Food Chem 65: 3609–3616.
– reference: 21. Lee KJ, Wui SU, Heo J, Kim SH, Jeong JY, Lee JB. 2003. DDT reduced testosterone and aromatase activity via ER receptor in leydig cell. Environ Anal Health Toxicol 18: 95–100.
– reference: 43. Wagner M, Halilbasic E, Marschall HU, Zollner G, Fickert P, Langner C, Zatloukal K, Denk H, Trauner M. 2005. CAR and PXR agonists stimulate hepatic bile acid and bilirubin detoxification and elimination pathways in mice. Hepatology 42: 420–430.
– reference: 34. Rogan WJ, Chen A. 2005. Health risks and benefits of bis(4-chlorophenyl)-1,1,1-trichloroethane (DDT). Lancet 366: 763–773.
– reference: 11. Govere JM, Durrheim DN, Kunene S. 2002. Malaria trends in South Africa and Swaziland and the introduction of synthetic pyrethroids to replace DDT for malaria vector control. S Afr J Sci 98: 19–21.
– reference: 48. Yanagiba Y, Ito Y, Kamijima M, Gonzalez FJ, Nakajima T. 2009. Octachlorostyrene induces cytochrome P450, UDP-glucuronosyltransferase, and sulfotransferase via the aryl hydrocarbon receptor and constitutive androstane receptor. Toxicol Sci 111: 19–26.
– reference: 12. Harada T, Takeda M, Kojima S, Tomiyama N. 2016. Toxicity and carcinogenicity of dichlorodiphenyltrichloroethane (DDT). Toxicol Res 32: 21–33.
– reference: 16. Kawase A, Fujii A, Negoro M, Akai R, Ishikubo M, Komura H, Iwaki M. 2008. Differences in cytochrome P450 and nuclear receptor mRNA levels in liver and small intestines between SD and DA rats. Drug Metab Pharmacokinet 23: 196–206.
– reference: 36. Safe S. 2020. Recent advances in understanding endocrine disruptors: DDT and related compounds. Fac Rev 9: 7.
– reference: 7. Delport R, Bornman R, MacIntyre UE, Oosthuizen NM, Becker PJ, Aneck-Hahn NH, de Jager C. 2011. Changes in retinol-binding protein concentrations and thyroid homeostasis with nonoccupational exposure to DDT. Environ Health Perspect 119: 647–651.
– reference: 31. Petersson J, Schreiber O, Steege A, Patzak A, Hellsten A, Phillipson M, Holm L. 2007. eNOS involved in colitis-induced mucosal blood flow increase. Am J Physiol Gastrointest Liver Physiol 293: G1281–G1287.
– reference: 6. Buckley DB, Klaassen CD. 2009. Induction of mouse UDP-glucuronosyltransferase mRNA expression in liver and intestine by activators of aryl-hydrocarbon receptor, constitutive androstane receptor, pregnane X receptor, peroxisome proliferator-activated receptor α, and nuclear factor erythroid 2-related factor 2. Drug Metab Dispos 37: 847–856.
– reference: 33. Ramirez T, Daneshian M, Kamp H, Bois FY, Clench MR, Coen M, Donley B, Fischer SM, Ekman DR, Fabian E, Guillou C, Heuer J, Hogberg HT, Jungnickel H, Keun HC, Krennrich G, Krupp E, Luch A, Noor F, Peter E, Riefke B, Seymour M, Skinner N, Smirnova L, Verheij E, Wagner S, Hartung T, van Ravenzwaay B, Leist M. 2013. Metabolomics in toxicology and preclinical research. ALTEX 30: 209–225.
– reference: 19. Krause W. 1977. Influence of DDT, DDVP and malathion on FSH, LH and testosterone serum levels and testosterone concentration in testis. Bull Environ Contam Toxicol 18: 231–242.
– reference: 39. Schymanski EL, Jeon J, Gulde R, Fenner K, Ruff M, Singer HP, Hollender J. 2014. Identifying small molecules via high resolution mass spectrometry: communicating confidence. Environ Sci Technol 48: 2097–2098.
– reference: 25. Marouani N, Hallegue D, Sakly M, Benkhalifa M, ben Rhouma K, Tebourbi O. 2017. p,p’-DDT induces testicular oxidative stress-induced apoptosis in adult rats. Reprod Biol Endocrinol 15: 40.
– reference: 27. Michihara A, Anraku M, Abe A, Kinoshita H, Kamizaki Y, Tomida H, Akasaki K. 2011. Comparison of receptors and enzymes regulating cholesterol levels in liver between SHR/NDmcr-cp rats and normotensive Wistar Kyoto rats at ten weeks of age. Biol Pharm Bull 34: 1116–1119.
– reference: 10. Ferdinandusse S, Houten SM. 2006. Peroxisomes and bile acid biosynthesis. Biochim Biophys Acta 1763: 1427–1440.
– reference: 35. Russell DW. 2003. The enzymes, regulation, and genetics of bile acid synthesis. Annu Rev Biochem 72: 137–174.
– reference: 37. Salihovic S, Ganna A, Fall T, Broeckling CD, Prenni JE, van Bavel B, Lind PM, Ingelsson E, Lind L. 2016. The metabolic fingerprint of p,p′-DDE and HCB exposure in humans. Environ Int 88: 60–66.
– reference: 51. Zhu QN, Xie HM, Zhang D, Liu J, Lu YF. 2013. Hepatic bile acids and bile acid-related gene expression in pregnant and lactating rats. PeerJ 1: e143.
– reference: 50. Zhang X, Yang Y, Su J, Zheng X, Wang C, Chen S, Liu J, Lv Y, Fan S, Zhao A, Chen T, Jia W, Wang X. 2021. Age-related compositional changes and correlations of gut microbiome, serum metabolome, and immune factor in rats. Geroscience 43: 709–725.
– reference: 45. Williams GP, Darbre PD. 2019. Low-dose environmental endocrine disruptors, increase aromatase activity, estradiol biosynthesis and cell proliferation in human breast cells. Mol Cell Endocrinol 486: 55–64.
– reference: 32. Pikuleva IA, Waterman MR. 2013. Cytochromes p450: roles in diseases. J Biol Chem 288: 17091–17098.
– reference: 26. Mellert W, Kapp M, Strauss V, Wiemer J, Kamp H, Walk T, Looser R, Prokoudine A, Fabian E, Krennrich G, Herold M, van Ravenzwaay B. 2011. Nutritional impact on the plasma metabolome of rats. Toxicol Lett 207: 173–181.
– reference: 30. Pellicoro A, van den Heuvel FAJ, Geuken M, Moshage H, Jansen PLM, Faber KN. 2007. Human and rat bile acid-CoA:amino acid N-acyltransferase are liver-specific peroxisomal enzymes: implications for intracellular bile salt transport. Hepatology 45: 340–348.
– reference: 13. Hu X, Li S, Cirillo P, Krigbaum N, Tran V, Ishikawa T, La Merrill MA, Jones DP, Cohn B. 2020. Metabolome Wide Association Study of serum DDT and DDE in Pregnancy and Early Postpartum. Reprod Toxicol 92: 129–137.
– reference: 23. Liu J, Yang Y, Yang Y, Zhang Y, Liu W. 2011. Disrupting effects of bifenthrin on ovulatory gene expression and prostaglandin synthesis in rat ovarian granulosa cells. Toxicology 282: 47–55.
– reference: 20. La Merrill M, Karey E, Moshier E, Lindtner C, La Frano MR, Newman JW, Buettner C. 2014. Perinatal exposure of mice to the pesticide DDT impairs energy expenditure and metabolism in adult female offspring. PLoS One 9: e103337.
– ident: 5
  doi: 10.1016/j.envint.2017.12.039
– ident: 52
  doi: 10.3389/fendo.2019.00886
– ident: 43
  doi: 10.1002/hep.20784
– ident: 33
  doi: 10.14573/altex.2013.2.209
– ident: 44
  doi: 10.1021/acs.jafc.7b00292
– ident: 16
  doi: 10.2133/dmpk.23.196
– ident: 46
  doi: 10.1016/j.tox.2016.11.016
– ident: 39
  doi: 10.1021/es5002105
– ident: 29
  doi: 10.1292/jvms.19-0168
– ident: 34
  doi: 10.1016/S0140-6736(05)67182-6
– ident: 38
  doi: 10.1093/toxsci/kfl051
– ident: 1
  doi: 10.1007/s11306-010-0231-x
– ident: 41
  doi: 10.1016/j.taap.2006.02.015
– ident: 45
  doi: 10.1016/j.mce.2019.02.016
– ident: 18
  doi: 10.1038/375581a0
– ident: 28
  doi: 10.1016/S0006-2952(00)00281-1
– ident: 37
  doi: 10.1016/j.envint.2015.12.015
– ident: 6
  doi: 10.1124/dmd.108.024190
– ident: 14
  doi: 10.1002/jssc.200700601
– ident: 20
  doi: 10.1371/journal.pone.0103337
– ident: 23
  doi: 10.1016/j.tox.2011.01.007
– ident: 3
  doi: 10.1292/jvms.09-0397
– ident: 25
  doi: 10.1186/s12958-017-0259-0
– ident: 8
  doi: 10.1016/j.envint.2017.02.011
– ident: 7
  doi: 10.1289/ehp.1002616
– ident: 22
  doi: 10.1016/j.bbalip.2009.01.016
– ident: 31
  doi: 10.1152/ajpgi.00357.2007
– ident: 42
  doi: 10.1007/s10552-017-0854-6
– ident: 2
  doi: 10.1111/j.1742-7843.2009.00439.x
– ident: 50
  doi: 10.1007/s11357-020-00188-y
– ident: 12
  doi: 10.5487/TR.2016.32.1.021
– ident: 36
  doi: 10.12703/b/9-7
– ident: 27
  doi: 10.1248/bpb.34.1116
– ident: 13
  doi: 10.1016/j.reprotox.2019.05.059
– ident: 48
  doi: 10.1093/toxsci/kfp130
– ident: 9
  doi: 10.1289/EHP2129
– ident: 17
  doi: 10.1016/j.taap.2013.05.008
– ident: 26
  doi: 10.1016/j.toxlet.2011.08.013
– ident: 19
  doi: 10.1007/BF01686072
– ident: 32
  doi: 10.1074/jbc.R112.431916
– ident: 51
  doi: 10.7717/peerj.143
– ident: 4
  doi: 10.1111/j.2517-6161.1995.tb02031.x
– ident: 24
  doi: 10.1016/j.chemosphere.2021.131815
– ident: 40
  doi: 10.1016/j.chemosphere.2015.08.029
– ident: 11
– ident: 49
  doi: 10.1038/s41598-020-61767-9
– ident: 30
  doi: 10.1002/hep.21528
– ident: 15
  doi: 10.1016/j.etap.2018.02.004
– ident: 47
  doi: 10.1016/j.cbpc.2021.109173
– ident: 10
  doi: 10.1016/j.bbamcr.2006.09.001
– ident: 21
– ident: 35
  doi: 10.1146/annurev.biochem.72.121801.161712
SSID ssj0021469
Score 2.3410995
Snippet Dichlorodiphenyltrichloroethane (DDT) is an organochlorine insecticide used worldwide. Several studies have reported the toxic effects of DDT and its...
Dichlorodiphenyltrichloroethane (DDT) is an organochlorine insecticide used worldwide. Several studies have reported the toxic effects of DDT and its...
SourceID pubmedcentral
proquest
pubmed
crossref
jstage
SourceType Open Access Repository
Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage 236
SubjectTerms Animals
Animals, Wild
bile acid biosynthesis
Bile Acids and Salts
Biosynthesis
DDT
DDT - pharmacology
dichlorodiphenyltrichloroethane (DDT)
Environmental effects
Enzymes
Gene expression
Hormones
Liquid chromatography
Liver
Male
Mammals
Mass spectroscopy
Metabolites
Metabolomics
Pesticides
Rats
steroid hormone biosynthesis
Steroids
Toxicity
Toxicology
wild rat
Xenobiotics
Title Investigation of dichlorodiphenyltrichloroethane (DDT) on xenobiotic enzyme disruption and metabolomic bile acid biosynthesis in DDT-sprayed areas using wild rats
URI https://www.jstage.jst.go.jp/article/jvms/85/2/85_22-0490/_article/-char/en
https://www.ncbi.nlm.nih.gov/pubmed/36596564
https://www.proquest.com/docview/2786726082
https://www.proquest.com/docview/2760817523
https://pubmed.ncbi.nlm.nih.gov/PMC10017292
Volume 85
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
ispartofPNX Journal of Veterinary Medical Science, 2023, Vol.85(2), pp.236-243
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV3fb5RAEN7U6oMvRusvbG3WRBONoR4L7EKMMcbaVM351DN9Iwu7tDR30B53pvjn-Jf6DXCk19QnXy6EGY47ZnbnG3b2G8ZeBlaNjNLSNZ4vXeBb46bCBq4UJrCe8o1p2fbHP-ThJPh2HB5vsFW30f4B1jemdtRPajKf7l1eNB8x4D-03AixeHf2a1bvIaeiRaxb7DZikqIhOg6G9QTqXt2x7nnSVYj6fQn89avXgtOdM-CzE3sT9LxeQXklJB3cZ_d6LMk_dcZ_wDZsucW2flKBS7vLlo_7hfOH7M8VPo2q5FXOITlFrl6Zgqq8mikx9bcnLL1Mt_z1_v7RGw7dS1sSVRPuwW35u5lZXFrPl-1Uw3Vp-Mwu4ElT2t7MU0wyXGeFwVFVNyXgZV3UvCg5vs6tz-e6sYZrqoTnVHJ_woHVDYcb1o_Y5ODL0edDt2_P4GYI6gtXSYAvFWtMUVrmXq6pqzoAYO6PrCeNiqMgi03q-ToiEp4sz5BbIQEyGTCjwPnHbLOsSvuUceP7odKwUWBFkI1SopSBkygTGe3rcOSwtyu7JFnPXU4tNKYJ5TCwYkJWTIRIyIoOezVon3ecHf_Qe9-ZeNDqR2unFYWJaD867UFI2-EwpzhsZ-UXycptE6EiqZAiRsJhLwYxRiwtw8B41ZJ0IAdqE77DnnRuNPwAX4YxEHbgsGjNwQYFYgNfl5TFacsK7rXpfCye_de_2mZ3BWBc95Jph20u5kv7HLBrke4i4fj6fbcdV38BxJ40CA
linkProvider Scholars Portal
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Investigation+of+dichlorodiphenyltrichloroethane+%28DDT%29+on+xenobiotic+enzyme+disruption+and+metabolomic+bile+acid+biosynthesis+in+DDT-sprayed+areas+using+wild+rats&rft.jtitle=Journal+of+Veterinary+Medical+Science&rft.au=SMIT%2C+Nico+J&rft.au=WEPENER%2C+Victor&rft.au=YOHANNES%2C+Yared+Beyene&rft.au=NAKAYAMA%2C+Shouta+MM&rft.date=2023&rft.pub=JAPANESE+SOCIETY+OF+VETERINARY+SCIENCE&rft.issn=0916-7250&rft.eissn=1347-7439&rft.volume=85&rft.issue=2&rft.spage=236&rft.epage=243&rft_id=info:doi/10.1292%2Fjvms.22-0490&rft.externalDocID=article_jvms_85_2_85_22_0490_article_char_en
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0916-7250&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0916-7250&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0916-7250&client=summon