Prenatal cannabis exposure and infant outcomes: Overview of studies

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 52, Issue , 2014, Pages 45-52

  Huizink, A C ^a,b  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Behavior; Fetal growth; Infancy; Prenatal cannabis exposure; Review

Indexed keywords

CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CANNABIS;

AGGRESSION; ARTICLE; ATTENTION DISTURBANCE; BEHAVIOR DISORDER; BRAIN DEVELOPMENT; CANNABIS SMOKING; CANNABIS USE; CHILD BEHAVIOR; COGNITIVE DEFECT; COGNITIVE DEVELOPMENT; DEVELOPMENTAL STAGE; FETUS DEVELOPMENT; FETUS GROWTH; FETUS OUTCOME; HEAD CIRCUMFERENCE; HIGH RISK INFANT; HUMAN; INFANT; INTRACELLULAR SIGNALING; INTRAUTERINE GROWTH RETARDATION; LONGITUDINAL STUDY; LOW BIRTH WEIGHT; MATERNAL BEHAVIOR; MATERNAL SMOKING; MEMORY DISORDER; MENTAL DEVELOPMENT; NEUROTRANSMISSION; NEWBORN ASSESSMENT; NONHUMAN; OUTCOME ASSESSMENT; PREGNANCY OUTCOME; PRENATAL EXPOSURE; PRENATAL PERIOD; RISK ASSESSMENT; SLEEP PATTERN; ANIMAL; CHEMICALLY INDUCED; CHILD DEVELOPMENT; COMPLICATION; DEVELOPMENTAL DISABILITIES; DISEASE MODEL; DRUG EFFECTS; FEMALE; MALE; PATHOPHYSIOLOGY; PREGNANCY;

ANIMALS; CANNABIS; CHILD DEVELOPMENT; DEVELOPMENTAL DISABILITIES; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; INFANT; LONGITUDINAL STUDIES; MALE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84899629766     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2013.09.014     Document Type: Article

References (80)

1. Annau Z., Eccles C.U. Prenatal exposure. Neurobehavioral toxicology 1986, Johns Hopkins University Press, Baltimore, MD. Z. Annau (Ed.).
2. Barker D.J.P. In utero programming of chronic disease. Clin Sci 1998, 95:115-128.
3. Barker D.J.P. Developmental origins of chronic disease. Public Health 2012, 126:185-189.
4. Barr H.M., Darby B.L., Streissguth A.P., Sampson P.D. Prenatal exposure to alcohol, caffeine, tobacco, and aspirin - effects on fine and gross motor-performance in 4-year-old children. Dev Psychol 1990, 26:339-348.
5. Boito S., Struijk P.C., Ursem N.T.C., Stijnen T., Wladimiroff J.W. Umbilical venous volume flow in the normally developing and growth-restricted human fetus. Ultrasound Obstet Gynecol 2002, 19:344-349.
6. Borgen L.A., Davis W.M. Vehicle and route of administration as parameters affecting operant behavioral effects of delta-9 tetrahydrocannabinol. J Pharm Sci 1973, 62:479-480.
7. Campolongo P., Trezza V., Palmery M., Trabace L., Cuomo V. Developmental exposure to cannabinoids causes subtle and enduring neurofunctional alterations. Int Rev Neurobiol 2009, 85:117-133.
8. Day N.L., Richardson G.A. Prenatal marijuana use - epidemiology, methodologic issues, and infant outcome. Clin Perinatol 1991, 18:77-91.
9. Day N., Sambamoorthi U., Taylor P., Richardson G., Robles N., Jhon Y., et al. Prenatal marijuana use and neonatal outcome. Neurotoxicol Teratol 1991, 13:329-334.
10. Day N.L., Richardson G.A., Goldschmidt L., Robles N., Taylor P.M., Stoffer D.S., et al. Effect of prenatal marijuana exposure on the cognitive-development of offspring at age-3. Neurotoxicol Teratol 1994, 16:169-175.
11. Defonseca F.R., Cebeira M., Fernandezruiz J.J., Navarro M., Ramos J.A. Effects of prenatal and perinatal exposure to hashish extracts on the ontogeny of brain dopaminergic-neurons. Neuroscience 1991, 43:713-723.
12. D'Onofrio B.M., Van Hulle C.A., Waldman I.D., Rodgers J.L., Harden K.P., Rathouz P.J., et al. Smoking during pregnancy and offspring externalizing problems: an exploration of genetic and environmental confounds. Dev Psychopathol 2008, 20:139-164.
13. Driscoll C.D., Streissguth A.P., Riley E.P. Prenatal alcohol exposure - comparability of effects in humans and animal-models. Neurotoxicol Teratol 1990, 12:231-237.
14. Ebrahim S.H., Gfroerer J. Pregnancy-related substance use in the United States during 1996-1998. Obstet Gynecol 2003, 101:374-379.
15. El Marroun H. Prenatal cannabis exposure and infant development: a tolerated matter 2010, (PhD thesis), Erasmus University, Rotterdam.
16. El Marroun H., Tiemeier H., Jaddoe V.W.V., Hofman A., Mackenbach J.P., Steegers E.A.P., et al. Demographic, emotional and social determinants of cannabis use in early pregnancy: the Generation R study. Drug Alcohol Depend 2008, 98:218-226.
17. El Marroun H., Tiemeier H., Steegers E.A.P., Jaddoe V.W.V., Hofman A., Verhulst F.C., et al. Intrauterine cannabis exposure affects fetal growth trajectories: the Generation R Study. J Am Acad Child Psychiatry 2009, 48:1173-1181.
18. El Marroun H., Tiemeier H., Steegers E.A.P., Roos-Hesselink J.W., Jaddoe V.W.V., Hofman A., et al. A prospective study on intrauterine cannabis exposure and fetal blood flow. Early Hum Dev 2010, 86:231-236.
19. El Marroun H., Hudziak J.J., Tiemeier H., Creemers H., Steegers E.A.P., Jaddoe V.W.V., et al. Intrauterine cannabis exposure leads to more aggressive behavior and attention problems in 18-month-old girls. Drug Alcohol Depend 2011, 118:470-474.
20. Ernst M., Moolchan E.T., Robinson M.L. Behavioral and neural consequences of prenatal exposure to nicotine. J Am Acad Child Psychiatry 2001, 40:630-641.
21. Fergusson D.M., Horwood L.J., Northstone K., Team A.L.S.P.A.C. Maternal use of cannabis and pregnancy outcome. BJOG 2002, 109:21-27.
22. Fried P.A. Short and long-term effects of prenatal cannabis inhalation upon rat offspring. Psychopharmacology (Berl) 1976, 50:285-291.
23. Fried P.A. Marihuana use by pregnant-women - neuro-behavioral effects in neonates. Drug Alcohol Depend 1980, 6:415-424.
24. Fried P.A. Adolescents prenatally exposed to marijuana: examination of facets of complex behaviors and comparisons with the influence of in utero cigarettes. J Clin Pharmacol 2002, 42:97S-102S.
25. Fried P.A. Conceptual issues in behavioral teratology and their application in determining long-term sequelae of prenatal marihuana exposures. J Child Psychol Psychiatry 2002, 43:81-102.
26. Fried P.A., O'Connell C.M. A comparison of the effects of prenatal exposure to tobacco, alcohol, cannabis and caffeine on birth size and subsequent growth. Neurotoxicol Teratol 1987, 9:79-85.
27. Fried P.A., Watkinson B. 12-Month and 24-month neurobehavioural follow-up of children prenatally exposed to marihuana, cigarettes and alcohol. Neurotoxicol Teratol 1988, 10:305-313.
28. Fried P.A., Watkinson B. 36-Month and 48-month neurobehavioral follow-up of children prenatally exposed to marijuana, cigarettes, and alcohol. J Dev Behav Pediatr 1990, 11:49-58.
29. Fried P.A., Watkinson B. Visuoperceptual functioning differs in 9- to 12-year olds prenatally exposed to cigarettes and marihuana. Neurotoxicol Teratol 2000, 22:11-20.
30. Fried P.A., Watkinson B., Gray R. Differential effects on cognitive functioning in 9- to 12-year olds prenatally exposed to cigarettes and marihuana. Neurotoxicol Teratol 1998, 20:293-306.
31. Fried P.A., Watkinson B., Willan A. Marijuana use during pregnancy and decreased length of gestation. Am J Obstet Gynecol 1984, 150:23-27.
32. Fried P.A., Watkinson B., Gray R. A follow-up-study of attentional behavior in 6-year-old children exposed prenatally to marijuana, cigarettes, and alcohol. Neurotoxicol Teratol 1992, 14:299-311.
33. Fried P.A., Watkinson B., Gray R. Differential effects on cognitive functioning in 9- to 12-year olds prenatally exposed to cigarettes and marihuana. Neurotoxicol Teratol 1998, 20:293-306.
34. Fried P., Watkinson B., James D., Gray F. Current and former marijuana use: preliminary findings of a longitudinal study of effects on IQ in young adults. Can Med Assoc J 2002, 166:887-891.
35. Fried P.A., Watkinson B., Gray R. Differential effects on cognitive functioning in 13- to 16-year-olds prenatally exposed to cigarettes and marihuana. Neurotoxicol Teratol 2003, 25:427-436.
36. Galve-Roperh I., Palazuelos J., Aguado T., Guzman M. The endocannabinoid system and the regulation of neural development: potential implications in psychiatric disorders. Eur Arch Psychiatry Clin Neurosci 2009, 259:371-382.
37. Gibson G.T., Baghurst P.A., Colley D.P. Maternal alcohol, tobacco and cannabis consumption and the outcome of pregnancy. Aust N Z J Obstet Gynaecol 1983, 23:15-19.
38. Glass M., Dragunow M., Faull R.L.M. Cannabinoid receptors in the human brain: a detailed anatomical and quantitative autoradiographic study in the fetal, neonatal and adult human brain. Neuroscience 1997, 77:299-318.
39. Goldschmidt L., Day N.L., Richardson G.A. Effects of prenatal marijuana exposure on child behavior problems at age 10. Neurotoxicol Teratol 2000, 22:325-336.
40. Goldschmidt L., Richardson G.A., Cornelius M.D., Day N.L. Prenatal marijuana and alcohol exposure and academic achievement at age 10. Neurotoxicol Teratol 2004, 26:521-532.
41. Gomez M., Hernandez M., Johansson B., de Miguel R., Ramos J.A., Fernandez-Ruiz J. Prenatal cannabinoid exposure and gene expression for neural adhesion molecule L1 in the fetal rat brain. Dev Brain Res 2003, 147:201-207.
42. Hadders-Algra M., Nakae Y., Vaneykern L.A., Klip-Van den Nieuwendijk A.W.J., Prechtl H.F.R. The effect of behavioral state on general movements in healthy full-term newborns - a polymyographic study. Early Hum Dev 1993, 35:63-79.
43. Hadlock F.P., Harrist R.B., Carpenter R.J., Deter R.L., Park S.K. Sonographic estimation of fetal weight - the value of femur length in addition to head and abdomen measurements. Radiology 1984, 150:535-540.
44. Harkany T., Guzman M., Galve-Roperh I., Berghuis P., Devi L.A., Mackie K. The emerging functions of endocannabinoid signaling during CNS development. Trends Pharmacol Sci 2007, 28:83-92.
45. Hatch E.E., Bracken M.B. Effect of marijuana use in pregnancy on fetal growth. Am J Epidemiol 1986, 124:986-993.
46. Helliwell R.J.A., Chamley L.W., Blake-Palmer K., Mitchell M.D., Wu J., Kearn C.S., et al. Characterization of the endocannabinoid system in early human pregnancy. J Clin Endocrinol Metab 2004, 89:5168-5174.
47. Hofman A., Jaddoe V.W.V., Mackenbach J.P., Moll H.A., Snijders R.F.M., Steegers E.A.P., et al. Growth, development and health from early fetal life until young adulthood: the Generation R Study. Paediatr Perinat Epidemiol 2004, 18:61-72.
48. Huizink A.C. Moderate use of alcohol, tobacco and cannabis during pregnancy: new approaches and update on research findings. Reprod Toxicol 2009, 28:143-151.
49. Huizink A.C., Mulder E.J.H. Maternal smoking, drinking or cannabis use during pregnancy and neurobehavioral and cognitive functioning in human offspring. Neurosci Biobehav Rev 2006, 30:24-41.
50. Hurd Y.L., Wang X., Anderson V., Beck O., Minkoff H., Dow-Edwards D. Marijuana impairs growth in mid-gestation fetuses. Neurotoxicol Teratol 2005, 27:221-229.
51. Hutchings D.E., Martin B.R., Gamagaris Z., Miller N., Fico T. Plasma-concentrations of delta-9-tetrahydrocannabinol in dams and fetuses following acute or multiple prenatal dosing in rats. Life Sci 1989, 44:697-701.
52. Jaddoe V.W.V., van Duijn C.M., Franco O.H., van der Heijden A.J., van IIzendoorn M.H., de Jongste J.C., et al. The Generation R Study: design and cohort update 2012. Eur J Epidemiol 2012, 27:739-756.
53. Jutras-Aswad D., DiNieri J.A., Harkany T., Hurd Y.L. Neurobiological consequences of maternal cannabis on human fetal development and its neuropsychiatric outcome. Eur Arch Psychiatry Clin Neurosci 2009, 259:395-412.
54. Knopik V.S. Maternal smoking during pregnancy and child outcomes: real or spurious effect?. Dev Neuropsychol 2009, 34:1-36.
55. Leech S.L., Richardson G.A., Goldschmidt L., Day N.L. Prenatal substance exposure: effects on attention and impulsivity of 6-year-olds. Neurotoxicol Teratol 1999, 21:109-118.
56. Lenard H.G., Vonbernu H., Prechtl H.F.R. Reflexes and their relationship to behavioural state in newborn. Acta Paediatr Scand 1968, 57:177-185.
57. Linn S., Schoenbaum S.C., Monson R.R., Rosner R., Stubblefield P.C., Ryan K.J. The association of marijuana use with outcome of pregnancy. Am J Public Health 1983, 73:1161-1164.
58. Linnet K.M., Dalsgaard S., Obel C., Wisborg K., Henriksen T.B., Rodriguez A., et al. Maternal lifestyle factors in pregnancy risk of attention deficit hyperactivity disorder and associated behaviors: review of the current evidence. Am J Psychiatry 2003, 160:1028-1040.
59. Little B.B., VanBeveren T.T. Placental transfer of selected substances of abuse. Semin Perinatol 1996, 20:147-153.
60. Mehmedic Z., Chandra S., Slade D., Denham H., Foster S., Patel A.S., et al. Potency trends of delta 9-THC and other cannabinoids in confiscated cannabis preparations from 1993 to 2008. J Forensic Sci 2010, 55:1209-1217.
61. Mereu G., Fa M., Ferraro L., Cagiano R., Antonelli T., Tattoli M., et al. Prenatal exposure to a cannabinoid agonist produces memory deficits linked to dysfunction in hippocampal long-term potentiation and glutamate release. Proc Natl Acad Sci U S A 2003, 100:4915-4920.
62. Miller H.C., Hassanei K. Fetal malnutrition in white newborn infants - maternal factors. Pediatrics 1973, 52:504-512.
63. Morris C.V., DiNieri J.A., Szutorisz H., Hurd Y.L. Molecular mechanisms of maternal cannabis and cigarette use on human neurodevelopment. Eur J Neurosci 2011, 34:1574-1583.
64. Navarro M., Rubio P., deFonseca F.R. Behavioural consequences of maternal exposure to natural cannabinoids in rats. Psychopharmacology (Berl) 1995, 122:1-14.
65. Park B., Gibbons H.M., Mitchell M.D., Glassa M. Identification of the CB1 cannabinoid receptor and fatty acid amide hydrolase (FAAH) in the human placenta. Placenta 2003, 24:473-478.
66. Pijlman F.T.A., Rigter S.M., Hoek J., Goldschmidt H.M.J., Niesink R.J.M. Strong increase in total delta-THC in cannabis preparations sold in Dutch coffee shops. Addict Biol 2005, 10:171-180.
67. Reece E.A., Goldstein I., Pilu G., Hobbins J.C. Fetal cerebellar growth unaffected by intrauterine growth-retardation - a new parameter for prenatal-diagnosis. Am J Obstet Gynecol 1987, 157:632-638.
68. Richardson G.A., Day N.L., Taylor P.M. The effect of prenatal alcohol, marijuana, and tobacco exposure on neonatal behavior. Infant Behav Dev 1989, 12:199-209.
69. Richardson G.A., Day N.L., Goldschmidt L. Prenatal alcohol, marijuana, and tobacco use - infant mental and motor development. Neurotoxicol Teratol 1995, 17:479-487.
70. Richardson G.A., Ryan C., Willford J., Day N.L., Goldschmidt L. Prenatal alcohol and marijuana exposure: effects on neuropsychological outcomes at 10years. Neurotoxicol Teratol 2002, 24:309-320.
71. Scher M.S., Richardson G.A., Coble P.A., Day N.L., Stoffer D.S. The effects of prenatal alcohol and marijuana exposure - disturbances in neonatal sleep cycling and arousal. Pediatr Res 1988, 24:101-105.
72. Smith A.M., Fried P.A., Hogan M.J. Cameron I. Effects of prenatal marijuana on response inhibition: an fMRI study of young adults. Neurotoxicol Teratol 2004, 26:533-542.
73. Streissguth A.P., Barr H.M., Sampson P.D. Moderate prenatal alcohol exposure - effects on child IQ and learning-problems at age 7 1/2years. Alcohol Clin Exp Res 1990, 14:662-669.
74. Thapar A., Rice F., Hay D., Boivin J., Langley K., van den Bree M., et al. Prenatal smoking might not cause attention-deficit/hyperactivity disorder: evidence from a novel design. Biol Psychiatry 2009, 66:722-727.
75. Trezza V., Campolongo P., Cassano T., Macheda T., Dipasquale P., Carratu M.R., et al. Effects of perinatal exposure to delta-9-tetrahydrocannabinol on the emotional reactivity of the offspring: a longitudinal behavioral study in Wistar rats. Psychopharmacology (Berl) 2008, 198:529-537.
76. Trezza V., Campolongo P., Manduca A., Morena M., Palmery M., Vanderschuren L.J.M.J., et al. Altering endocannabinoid neurotransmission at critical developmental ages: impact on rodent emotionality and cognitive performance. Front Behav Neurosci 2012, 6:2.
77. Vorhees C.V. Concepts in teratology and developmental toxicology derived from animal research. Annals NY. Acad. Sci. 1989, New York Academy of Sciences, New York, NY. D.E. Hutchings (Ed.).
78. Wang L., Liu H., Harvey-White J., Zimmer A., Kunos G. Endocannabinoid signaling via cannabinoid receptor 1 is involved in ethanol preference and its age-dependent decline in mice. Proc Natl Acad Sci U S A 2003, 100:1393-1398.
79. Wu C.S., Jew C.P., Lu H.C. Lasting impacts of prenatal cannabis exposure and the role of endogenous cannabinoids in the developing brain. Future Neurol. 2011, 6:459-480.
80. Zuckerman B., Frank D.A., Hingson R., Amaro H., Levenson S.M., Kayne H., et al. Effects of maternal marijuana and cocaine use on fetal growth. N Engl J Med 1989, 320:762-768.