{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,21]],"date-time":"2026-06-21T05:27:47Z","timestamp":1782019667149,"version":"3.54.5"},"reference-count":117,"publisher":"Wiley","issue":"12","license":[{"start":{"date-parts":[[2019,3,10]],"date-time":"2019-03-10T00:00:00Z","timestamp":1552176000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"funder":[{"DOI":"10.13039\/100000027","name":"National Institute on Alcohol Abuse and Alcoholism","doi-asserted-by":"publisher","award":["AA025425"],"award-info":[{"award-number":["AA025425"]}],"id":[{"id":"10.13039\/100000027","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Birth Defects Research"],"published-print":{"date-parts":[[2019,7,15]]},"abstract":"<jats:p>Cannabis is the most commonly used illicit drug among pregnant women. Moreover, over half of pregnant women who are consuming cannabis are also consuming alcohol; however, the consequences of combined prenatal alcohol and cannabis exposure on fetal development are not well understood. The current study examined behavioral development following exposure to ethanol (EtOH) and\/or CP\u201055,940 (CP), a cannabinoid receptor agonist. From postnatal days (PD) 4\u20139, a period of brain development equivalent to the third trimester, Sprague\u2013Dawley rats received EtOH (5.25\u2009g\/kg\/day) or sham intubation, as well as CP (0.4 mg\/kg\/day) or vehicle. All subjects were tested on open field activity (PD 18\u201321), elevated plus maze (PD 25), and spatial learning (PD 40\u201346) tasks. Both EtOH and CP increased locomotor activity in the open field, and the combination produced more severe overactivity than either exposure alone. Similarly, increases in thigmotaxis in the Morris water maze were caused by either EtOH or CP alone, and were more severe with combined exposure, although only EtOH impaired spatial learning. Finally, developmental CP significantly increased time spent in the open arms on the elevated plus maze. Overall, these data indicate that EtOH and CP produce some independent effects on behavior, and that the combination produces more severe overactivity in the open field. Importantly, these data suggest that prenatal cannabis disrupts development and combined prenatal exposure to alcohol and cannabis may be particularly damaging to the developing fetus, which has implications for the lives of affected individuals and families and also for establishing public health policy.<\/jats:p>","DOI":"10.1002\/bdr2.1487","type":"journal-article","created":{"date-parts":[[2019,3,11]],"date-time":"2019-03-11T01:09:59Z","timestamp":1552266599000},"page":"760-774","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":38,"title":["The effects of alcohol and cannabinoid exposure during the brain growth spurt on behavioral development in rats"],"prefix":"10.1002","volume":"111","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9996-9134","authenticated-orcid":false,"given":"Kristen R.","family":"Breit","sequence":"first","affiliation":[{"name":"Department of Psychology, Center for Behavioral Teratology San Diego State University  San Diego California"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brandonn","family":"Zamudio","sequence":"additional","affiliation":[{"name":"Department of Psychology, Center for Behavioral Teratology San Diego State University  San Diego California"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jennifer D.","family":"Thomas","sequence":"additional","affiliation":[{"name":"Department of Psychology, Center for Behavioral Teratology San Diego State University  San Diego California"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2019,3,10]]},"reference":[{"key":"e_1_2_7_2_1","doi-asserted-by":"publisher","DOI":"10.1016\/0024-3205(90)90374-Z"},{"key":"e_1_2_7_3_1","doi-asserted-by":"publisher","DOI":"10.1002\/tera.1420360206"},{"key":"e_1_2_7_4_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-1-4613-2189-7_12"},{"key":"e_1_2_7_5_1","volume-title":"The rat: A study in behavior","author":"Barnett S. A.","year":"1963"},{"key":"e_1_2_7_6_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1530-0277.1988.tb00133.x"},{"key":"e_1_2_7_7_1","doi-asserted-by":"publisher","DOI":"10.3390\/brainsci5040456"},{"key":"e_1_2_7_8_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1471-4159.2008.05685.x"},{"key":"e_1_2_7_9_1","doi-asserted-by":"publisher","DOI":"10.1016\/0892-0362(94)00053-G"},{"issue":"12","key":"e_1_2_7_10_1","first-page":"884","article-title":"Synthetic cannabinoids\u2013The new legal high drugs","volume":"150","author":"Berkovitz R.","year":"2011","journal-title":"Harefuah"},{"key":"e_1_2_7_11_1","doi-asserted-by":"publisher","DOI":"10.1002\/(SICI)1098-1063(2000)10:1<94::AID-HIPO11>3.0.CO;2-T"},{"key":"e_1_2_7_12_1","doi-asserted-by":"publisher","DOI":"10.1002\/(SICI)1098-2396(19990901)33:3<181::AID-SYN3>3.0.CO;2-R"},{"key":"e_1_2_7_13_1","doi-asserted-by":"publisher","DOI":"10.4088\/PCC.v09n0608"},{"key":"e_1_2_7_14_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00213-003-1550-7"},{"key":"e_1_2_7_15_1","doi-asserted-by":"publisher","DOI":"10.1016\/0091-3057(73)90100-7"},{"key":"e_1_2_7_16_1","unstructured":"Botticelli M.(2016).National drug control strategy: Data supplement 2015."},{"key":"e_1_2_7_17_1","unstructured":"Botticelli M.(2017).National drug control strategy: Data supplement 2016."},{"key":"e_1_2_7_18_1","doi-asserted-by":"crossref","unstructured":"Breit K. R. Zamudio B. &Thomas J. D.(2019). Altered motor development following late gestational alcohol and cannabinoid exposure in rats.https:\/\/doi.org\/10.1101\/513713.","DOI":"10.1101\/513713"},{"key":"e_1_2_7_19_1","unstructured":"Centers for Disease Control and Prevention. (2015).Fetal alcohol spectrum disorders (FASD)."},{"key":"e_1_2_7_20_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.472762"},{"key":"e_1_2_7_21_1","doi-asserted-by":"publisher","DOI":"10.1016\/0892-0362(91)90079-C"},{"key":"e_1_2_7_22_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0095-5108(18)30535-9"},{"key":"e_1_2_7_23_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1514962112"},{"key":"e_1_2_7_24_1","doi-asserted-by":"publisher","DOI":"10.1373\/clinchem.2013.216507"},{"key":"e_1_2_7_25_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0166-4328(98)00107-7"},{"key":"e_1_2_7_26_1","doi-asserted-by":"publisher","DOI":"10.1016\/0378-3782(79)90022-7"},{"issue":"2","key":"e_1_2_7_27_1","first-page":"374","article-title":"Pregnancy\u2010related substance use in the United States during 1996\u20131998","volume":"101","author":"Ebrahim S. H.","year":"2003","journal-title":"Obstetrics & Gynecology"},{"key":"e_1_2_7_28_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.drugalcdep.2011.03.004"},{"key":"e_1_2_7_29_1","doi-asserted-by":"publisher","DOI":"10.1097\/CHI.0b013e3181bfa8ee"},{"key":"e_1_2_7_30_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.lfs.2005.09.011"},{"issue":"3","key":"e_1_2_7_31_1","first-page":"1383","article-title":"Development of cross\u2010tolerance between delta 9\u2010tetrahydrocannabinol, CP 55,940 and WIN 55,212","volume":"271","author":"Fan F.","year":"1994","journal-title":"Journal of Pharmacology and Experimental Therapeutics"},{"key":"e_1_2_7_32_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.lfs.2013.09.017"},{"key":"e_1_2_7_33_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.drugalcdep.2018.09.018"},{"key":"e_1_2_7_34_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1471-0528.2002.01020.x"},{"key":"e_1_2_7_35_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0166-2236(99)01491-5"},{"issue":"9","key":"e_1_2_7_36_1","first-page":"688","article-title":"Alcohol exacerbates the teratogenic effects of prenatal cannabinoid exposure in a C57BL\/6J mouse model","volume":"109","author":"Fish E. W.","year":"2017","journal-title":"Birth Defects Research"},{"issue":"1","key":"e_1_2_7_37_1","first-page":"287A","article-title":"Ethanol and the synthetic cannabinoid, CP\u201055,940, are synergistically teratogenic in a mouse model","volume":"40","author":"Fish E. W.","year":"2016","journal-title":"Alcoholism: Clinical and Experimental Research"},{"key":"e_1_2_7_38_1","doi-asserted-by":"publisher","DOI":"10.1002\/bms.1200141104"},{"key":"e_1_2_7_39_1","doi-asserted-by":"publisher","DOI":"10.1016\/0165-3806(96)00087-9"},{"key":"e_1_2_7_40_1","doi-asserted-by":"publisher","DOI":"10.1016\/0892-0362(87)90082-1"},{"key":"e_1_2_7_41_1","doi-asserted-by":"publisher","DOI":"10.1016\/0892-0362(88)90032-3"},{"issue":"6","key":"e_1_2_7_42_1","first-page":"383","article-title":"60\u2010and 72\u2010month follow\u2010up of children prenatally exposed to marijuana, cigarettes, and alcohol: Cognitive and language assessment","volume":"13","author":"Fried P. A.","year":"1992","journal-title":"Journal of Developmental & Behavioral Pediatrics"},{"issue":"2","key":"e_1_2_7_43_1","first-page":"49","article-title":"36\u2010and 48\u2010month neurobehavioral follow\u2010up of children prenatally exposed to marijuana, cigarettes, and alcohol","volume":"11","author":"Fried P. A.","year":"1990","journal-title":"Journal of Developmental & Behavioral Pediatrics"},{"key":"e_1_2_7_44_1","doi-asserted-by":"publisher","DOI":"10.1093\/ilar.47.1.1"},{"key":"e_1_2_7_45_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ntt.2015.12.004"},{"key":"e_1_2_7_46_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1530-0277.2000.tb04611.x"},{"key":"e_1_2_7_47_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ntt.2014.01.007"},{"key":"e_1_2_7_48_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0892-0362(00)00066-0"},{"key":"e_1_2_7_49_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ntt.2004.04.003"},{"key":"e_1_2_7_50_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.devbrainres.2003.10.016"},{"key":"e_1_2_7_51_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0892-0362(97)00062-7"},{"key":"e_1_2_7_52_1","doi-asserted-by":"publisher","DOI":"10.1006\/nlme.1995.0009"},{"key":"e_1_2_7_53_1","doi-asserted-by":"publisher","DOI":"10.1016\/0892-0362(91)90029-V"},{"key":"e_1_2_7_54_1","doi-asserted-by":"publisher","DOI":"10.2165\/00003088-200342040-00003"},{"key":"e_1_2_7_55_1","doi-asserted-by":"publisher","DOI":"10.1002\/ana.21287"},{"key":"e_1_2_7_56_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-3016.2003.00521.x"},{"key":"e_1_2_7_57_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.pnpbp.2013.09.014"},{"key":"e_1_2_7_58_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neubiorev.2005.04.005"},{"key":"e_1_2_7_59_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ntt.2004.11.002"},{"key":"e_1_2_7_60_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ntt.2011.04.004"},{"key":"e_1_2_7_61_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10654-012-9735-1"},{"key":"e_1_2_7_62_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10654-010-9516-7"},{"key":"e_1_2_7_63_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00213-018-4946-0"},{"key":"e_1_2_7_64_1","doi-asserted-by":"publisher","DOI":"10.1016\/0166-4328(88)90121-0"},{"key":"e_1_2_7_65_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11065-015-9289-6"},{"key":"e_1_2_7_66_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0006-8993(02)02492-7"},{"key":"e_1_2_7_67_1","doi-asserted-by":"publisher","DOI":"10.1097\/WNR.0000000000000993"},{"key":"e_1_2_7_68_1","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2393-14-127"},{"key":"e_1_2_7_69_1","doi-asserted-by":"publisher","DOI":"10.1097\/FTD.0b013e318288453f"},{"key":"e_1_2_7_70_1","doi-asserted-by":"publisher","DOI":"10.1097\/FBP.0000000000000184"},{"key":"e_1_2_7_71_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11065-011-9167-9"},{"key":"e_1_2_7_72_1","doi-asserted-by":"publisher","DOI":"10.1016\/0091-3057(95)02066-7"},{"key":"e_1_2_7_73_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1556-4029.2010.01441.x"},{"key":"e_1_2_7_74_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0537849100"},{"key":"e_1_2_7_75_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1360-0443.1988.tb00526.x"},{"key":"e_1_2_7_76_1","doi-asserted-by":"publisher","DOI":"10.1124\/jpet.116.235630"},{"key":"e_1_2_7_77_1","doi-asserted-by":"publisher","DOI":"10.1007\/s40474-014-0020-8"},{"key":"e_1_2_7_78_1","doi-asserted-by":"publisher","DOI":"10.1111\/jnc.13006"},{"key":"e_1_2_7_79_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF02247471"},{"key":"e_1_2_7_80_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuropharm.2016.05.021"},{"key":"e_1_2_7_81_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1530-0277.2012.01880.x"},{"key":"e_1_2_7_82_1","doi-asserted-by":"publisher","DOI":"10.1097\/00008877-200509000-00019"},{"key":"e_1_2_7_83_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1750-3639.2002.tb00467.x"},{"key":"e_1_2_7_84_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1530-0277.1998.tb04312.x"},{"key":"e_1_2_7_85_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0165-3806(99)00170-4"},{"key":"e_1_2_7_86_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0014-2999(03)01272-X"},{"key":"e_1_2_7_87_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0892-0362(02)00193-9"},{"key":"e_1_2_7_88_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11065-011-9166-x"},{"key":"e_1_2_7_89_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0149-7634(96)00058-9"},{"key":"e_1_2_7_90_1","doi-asserted-by":"publisher","DOI":"10.1097\/00001756-199302000-00005"},{"key":"e_1_2_7_91_1","doi-asserted-by":"publisher","DOI":"10.1111\/acer.12939"},{"key":"e_1_2_7_92_1","doi-asserted-by":"publisher","DOI":"10.1038\/sj.npp.1301664"},{"key":"e_1_2_7_93_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.brainres.2008.08.048"},{"key":"e_1_2_7_94_1","unstructured":"Saint Louis C.(2017). Pregnant women turn to marijuana perhaps harming infants. The New York Times. Retrieved fromhttps:\/\/www.nytimes.com\/2017\/02\/02\/health\/marijuana-and-pregnancy.html?emc=eta1&_r=0"},{"key":"e_1_2_7_95_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00406-009-0026-0"},{"key":"e_1_2_7_96_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11065-011-9168-8"},{"key":"e_1_2_7_97_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ntt.2005.12.008"},{"key":"e_1_2_7_98_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.3786-12.2013"},{"key":"e_1_2_7_99_1","doi-asserted-by":"publisher","DOI":"10.1111\/acer.12698"},{"key":"e_1_2_7_100_1","unstructured":"Substance Abuse and Mental Health Services Administration. (2015).Behavioral health trends in the United States: Results from the 2014 national survey on drug use and health."},{"key":"e_1_2_7_101_1","unstructured":"Substance Use and Mental Health Services Administration. (2014).Results from the 2013 national survey on drug use and health: Summary of national findings."},{"key":"e_1_2_7_102_1","doi-asserted-by":"publisher","DOI":"10.1111\/bph.13024"},{"key":"e_1_2_7_103_1","doi-asserted-by":"publisher","DOI":"10.1007\/s40429-014-0014-y"},{"key":"e_1_2_7_104_1","doi-asserted-by":"publisher","DOI":"10.1002\/hbm.22620"},{"key":"e_1_2_7_105_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ntt.2009.07.002"},{"key":"e_1_2_7_106_1","doi-asserted-by":"publisher","DOI":"10.1037\/0735-7044.121.1.120"},{"key":"e_1_2_7_107_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ntt.2003.10.002"},{"key":"e_1_2_7_108_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0892-0362(00)00097-0"},{"key":"e_1_2_7_109_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0166-4328(00)00263-1"},{"key":"e_1_2_7_110_1","doi-asserted-by":"publisher","DOI":"10.3389\/fnbeh.2012.00002"},{"key":"e_1_2_7_111_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.psyneuen.2017.05.019"},{"key":"e_1_2_7_112_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.drugalcdep.2014.07.029"},{"key":"e_1_2_7_113_1","doi-asserted-by":"publisher","DOI":"10.1016\/0741-8329(92)90057-H"},{"key":"e_1_2_7_114_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2826.2008.01669.x"},{"key":"e_1_2_7_115_1","doi-asserted-by":"publisher","DOI":"10.1016\/0741-8329(84)90101-0"},{"key":"e_1_2_7_116_1","doi-asserted-by":"publisher","DOI":"10.1016\/0006-8993(90)90347-E"},{"key":"e_1_2_7_117_1","doi-asserted-by":"publisher","DOI":"10.1016\/0736-5748(89)90046-4"},{"key":"e_1_2_7_118_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0166-4328(05)80039-7"}],"container-title":["Birth Defects Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fbdr2.1487","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/bdr2.1487","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1002\/bdr2.1487","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/bdr2.1487","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,9]],"date-time":"2023-09-09T11:24:16Z","timestamp":1694258656000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/bdr2.1487"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,3,10]]},"references-count":117,"journal-issue":{"issue":"12","published-print":{"date-parts":[[2019,7,15]]}},"alternative-id":["10.1002\/bdr2.1487"],"URL":"https:\/\/doi.org\/10.1002\/bdr2.1487","archive":["Portico"],"relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/513796","asserted-by":"object"}]},"ISSN":["2472-1727","2472-1727"],"issn-type":[{"value":"2472-1727","type":"print"},{"value":"2472-1727","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,3,10]]},"assertion":[{"value":"2018-09-04","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2019-02-13","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2019-03-10","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}