0
Get Alert
Please Wait... Processing your request... Please Wait.
You must sign in to sign-up for alerts.

Please confirm that your email address is correct, so you can successfully receive this alert.

Articles   |    
Maternal Smoking During Pregnancy and Bipolar Disorder in Offspring
Ardesheer Talati, Ph.D.; Yuanyuan Bao, M.S.; Jake Kaufman, B.A.; Ling Shen, Ph.D.; Catherine A. Schaefer, Ph.D.; Alan S. Brown, M.D., M.P.H.
Am J Psychiatry 2013;170:1178-1185. doi:10.1176/appi.ajp.2013.12121500
View Author and Article Information

The authors report no financial relationships with commercial interests.

From the Department of Psychiatry, Columbia University, New York; the Division of Epidemiology, New York State Psychiatric Institute, New York; Kaiser Permanente Division of Research, Oakland, Calif.; and the Department of Epidemiology, Columbia University Mailman School of Public Health, New York.

Address correspondence to Dr. Talati (at2071@columbia.edu).

Supported by NIMH (grants 5R01-MH073080-05 and 5K02-MH65422 to A.S.B. and 5R01-MH069819 to C.A.S.), the National Institute of Drug Abuse (K01DA029598 to A.T.), and Young Investigator Grants from NARSAD.

Copyright © 2013 by the American Psychiatric Association

Received December 01, 2012; Revised February 28, 2013; Revised March 29, 2013; Accepted April 08, 2013.

Abstract

Objective  Maternal smoking during pregnancy is associated with a number of adverse externalizing outcomes for offspring from childhood to adulthood. The relationship between maternal smoking and bipolar disorder in offspring, which includes externalizing symptoms among its many manifestations, has not been investigated in depth. The authors examined whether offspring exposed to maternal smoking in utero would be at increased lifetime risk for bipolar disorder after accounting for other factors related to maternal smoking.

Method  Individuals with bipolar disorder (N=79) were ascertained from the birth cohort of the Child Health and Development Study. Case subjects were identified by a combination of clinical, database, and direct mailing sources; all case subjects were directly interviewed and diagnosed using DSM-IV criteria. Comparison subjects (N=654) were matched to case subjects on date of birth (±30 days), sex, membership in the cohort at the time of illness onset, and availability of maternal archived sera.

Results  After adjusting for potential confounders, offspring exposed to in utero maternal smoking exhibited a twofold greater risk for bipolar disorder (odds ratio=2.014, 95% confidence interval=1.48–2.53, p=0.01). The associations were noted primarily among bipolar offspring without psychotic features.

Conclusions  Prenatal tobacco exposure may be one suspected cause of bipolar disorder. However, it will be necessary to account for other unmeasured familial factors before causal teratogenic effects can be suggested.

Abstract Teaser
Figures in this Article

Your Session has timed out. Please sign back in to continue.
Sign In Your Session has timed out. Please sign back in to continue.
Sign In to Access Full Content
 
Username
Password
Sign in via Athens (What is this?)
Athens is a service for single sign-on which enables access to all of an institution's subscriptions on- or off-site.
Not a subscriber?

Subscribe Now/Learn More

PsychiatryOnline subscription options offer access to the DSM-5 library, books, journals, CME, and patient resources. This all-in-one virtual library provides psychiatrists and mental health professionals with key resources for diagnosis, treatment, research, and professional development.

Need more help? PsychiatryOnline Customer Service may be reached by emailing PsychiatryOnline@psych.org or by calling 800-368-5777 (in the U.S.) or 703-907-7322 (outside the U.S.).

FIGURE 1. Flow Chart for Identification of Case Subjects With Bipolar Disorder in a Study of Maternal Smoking During Pregnancy

a Individuals who could not be interviewed (N=54) included deceased or incarcerated individuals, those without permission from a physician, or those too ill (psychosis or severe mental disability).

b Interviewed and noninterviewed cases did not differ by exposure status (46% exposed compared with 42.4% unexposed during pregnancy; p=0.47).

c One case subject was excluded because he or she was the sibling of another. Fifteen case subjects lacking data on maternal prenatal smoking were removed, along with their matched comparison subjects. The final sample thus contained 79 case and 654 matched comparison subjects. Of the 79 case subjects, 66 (83.5%) had bipolar I disorder, 10 (12.6%) had bipolar II disorder, and three (3.8%) had bipolar disorder not otherwise specified. Bipolar disorder with psychotic features was diagnosed in 33 case subjects.

Anchor for Jump
TABLE 1.Maternal and Offspring Demographic Characteristics and Pregnancy-Related History by Maternal Smoking Status
Table Footer Note

a Severe psychiatric history includes lifetime diagnoses of schizophrenia or other psychotic disorders, affective disorder, and postpartum depression.

Table Footer Note

b Any psychiatric history includes any anxiety, emotional problems, psychoneuroses, hypochondriasis, neurasthenia, alcoholism, drug addiction or habituation, mental deficiency, or mental disorders.

Table Footer Note

c Included use of thioridazine, fluphenazine, trifluoperazine, chlorpromazine, perphenazine, haloperidol, or lithium carbonate.

Table Footer Note

d Alcohol use was defined as having at least one bottle or glass of beer, wine, or whisky per week. There were 93 mothers (12.7%) who were missing data on alcohol use during pregnancy (15.3% of those who smoked during pregnancy versus 10.7% of those who did not; χ2=3.4, p=0.07).

Table Footer Note

e Caffeine use was defined as having one or more cups of coffee daily during pregnancy. Mean number of cups per day among nonsmoking and smoking mothers were 2.5 and 4.2, respectively (t=7.7, p<0.001).

Table Footer Note

f Two offspring were missing data on premature delivery.

Anchor for Jump
TABLE 2.Maternal and Offspring Demographic Characteristics and Pregnancy-Related History by Bipolar Disorder in Offspring
Table Footer Note

a Severe psychiatric history includes lifetime diagnoses of schizophrenia or other psychotic disorders, affective disorder, and postpartum depression.

Table Footer Note

b Any psychiatric history includes any anxiety, emotional problems, psychoneuroses, hypochondriasis, neurasthenia, alcoholism, drug addiction or habituation, mental deficiency, or mental disorders

Table Footer Note

c Included use of thioridazine, fluphenazine, trifluoperazine, chlorpromazine, perphenazine, haloperidol, or lithium carbonate.

Table Footer Note

d Alcohol use was defined as having at least one bottle or glass of beer, wine, or whisky per week. There were 93 offspring (12.7%) missing maternal data on alcohol exposure during pregnancy (8.9% of those with versus 13.1% of those without a diagnosis of bipolar disorder; χ2=1.2, p=0.27).

Table Footer Note

e Caffeine use was defined as having one or more cups of coffee daily during pregnancy. Bipolar disorder status in offspring status also did not vary by number of cups the mother drank per day while pregnant (3.1 daily for mothers of case subjects and 3.7 for mothers of comparison subjects (t=1.47, p=0.14).

Table Footer Note

f Two offspring were missing data on premature delivery.

Anchor for Jump
TABLE 3.Associations Between Maternal Smoking During Pregnancy and Bipolar Disorder in Offspring
Table Footer Note

a Lifetime psychopathology includes any anxiety, emotional problems, psychoneuroses, hypochondriasis, neurasthenia, alcoholism, drug addiction or habituation, mental deficiency, or mental disorders. Lifetime severe psychopathology includes lifetime diagnoses of schizophrenia or other psychotic disorders, affective disorder, and postpartum depression.

+

References

Centers for Disease Control:  Maternal and Infant Health: Smoking During Pregnancy .  Atlanta,  Centers for Disease Control and Prevention, Department of Health and Human Services, 2006
 
Ananth  CV;  Smulian  JC;  Vintzileos  AM:  Incidence of placental abruption in relation to cigarette smoking and hypertensive disorders during pregnancy: a meta-analysis of observational studies.  Obstet Gynecol 1999; 93:622–628
[CrossRef] | [PubMed]
 
Hunter  SK;  Kisley  MA;  McCarthy  L;  Freedman  R;  Ross  RG:  Diminished cerebral inhibition in neonates associated with risk factors for schizophrenia: parental psychosis, maternal depression, and nicotine use.  Schizophr Bull 2011; 37:1200–1208
[CrossRef] | [PubMed]
 
Nigg  JT;  Breslau  N:  Prenatal smoking exposure, low birth weight, and disruptive behavior disorders.  J Am Acad Child Adolesc Psychiatry 2007; 46:362–369
[CrossRef] | [PubMed]
 
Ekblad  M;  Gissler  M;  Lehtonen  L;  Korkeila  J:  Prenatal smoking exposure and the risk of psychiatric morbidity into young adulthood.  Arch Gen Psychiatry 2010; 67:841–849
[CrossRef] | [PubMed]
 
Weissman  MM;  Warner  V;  Wickramaratne  PJ;  Kandel  DB:  Maternal smoking during pregnancy and psychopathology in offspring followed to adulthood.  J Am Acad Child Adolesc Psychiatry 1999; 38:892–899
[CrossRef] | [PubMed]
 
Mauricio Tohen  JA (ed):  The Epidemiology of Bipolar Disorder, 3rd ed .  New York,  Wiley, 2011
 
Serrano  E;  Ezpeleta  L;  Castro-Fornieles  J:  Comorbidity and phenomenology of bipolar disorder in children with ADHD.  J Atten Disord 2013; 17:330–338
[CrossRef] | [PubMed]
 
Heffner  JL;  Strawn  JR;  DelBello  MP;  Strakowski  SM;  Anthenelli  RM:  The co-occurrence of cigarette smoking and bipolar disorder: phenomenology and treatment considerations.  Bipolar Disord 2011; 13:439–453
[CrossRef] | [PubMed]
 
Kreinin  A;  Novitski  D;  Rabinowitz  D;  Weizman  A;  Grinshpoon  A:  Association between tobacco smoking and bipolar affective disorder: clinical, epidemiological, cross-sectional, retrospective study in outpatients.  Compr Psychiatry 2012; 53:269–274
[CrossRef] | [PubMed]
 
Moore  PB;  El-Badri  SM;  Cousins  D;  Shepherd  DJ;  Young  AH;  McAllister  VL;  Ferrier  IN:  White matter lesions and season of birth of patients with bipolar affective disorder.  Am J Psychiatry 2001; 158:1521–1524
[CrossRef] | [PubMed]
 
Susser  ES;  Schaefer  CA;  Brown  AS;  Begg  MD;  Wyatt  RJ:  The design of the prenatal determinants of schizophrenia study.  Schizophr Bull 2000; 26:257–273
[CrossRef] | [PubMed]
 
Nurnberger  JI  Jr;  Blehar  MC;  Kaufmann  CA;  York-Cooler  C;  Simpson  SG;  Harkavy-Friedman  J;  Severe  JB;  Malaspina  D;  Reich  T  (NIMH Genetics Initiative): Diagnostic Interview for Genetic Studies: rationale, unique features, and training. Arch Gen Psychiatry 1994; 51:849–859
 
Williams  GM;  O’Callaghan  M;  Najman  JM;  Bor  W;  Andersen  MJ;  Richards  D;  U  C:  Maternal cigarette smoking and child psychiatric morbidity: a longitudinal study.  Pediatrics 1998; 102:e11
[CrossRef] | [PubMed]
 
Ekblad  M;  Gissler  M;  Lehtonen  L;  Korkeila  J:  Relation of prenatal smoking exposure and use of psychotropic medication up to young adulthood.  Am J Epidemiol 2011; 174:681–690
[CrossRef] | [PubMed]
 
Wakschlag  LS;  Lahey  BB;  Loeber  R;  Green  SM;  Gordon  RA;  Leventhal  BL:  Maternal smoking during pregnancy and the risk of conduct disorder in boys.  Arch Gen Psychiatry 1997; 54:670–676
[CrossRef] | [PubMed]
 
Kovacs  M;  Pollock  M:  Bipolar disorder and comorbid conduct disorder in childhood and adolescence.  J Am Acad Child Adolesc Psychiatry 1995; 34:715–723
[CrossRef] | [PubMed]
 
Skirrow  C;  Hosang  GM;  Farmer  AE;  Asherson  P:  An update on the debated association between ADHD and bipolar disorder across the lifespan.  J Affect Disord 2012; 141:143–159
[CrossRef] | [PubMed]
 
Biederman  J;  Petty  CR;  Byrne  D;  Wong  P;  Wozniak  J;  Faraone  SV:  Risk for switch from unipolar to bipolar disorder in youth with ADHD: a long term prospective controlled study.  J Affect Disord 2009; 119:16–21
[CrossRef] | [PubMed]
 
Hirshfeld-Becker  DR;  Biederman  J;  Henin  A;  Faraone  SV;  Dowd  ST;  De Petrillo  LA;  Markowitz  SM;  Rosenbaum  JF:  Psychopathology in the young offspring of parents with bipolar disorder: a controlled pilot study.  Psychiatry Res 2006; 145:155–167
[CrossRef] | [PubMed]
 
Wozniak  J;  Faraone  SV;  Mick  E;  Monuteaux  M;  Coville  A;  Biederman  J:  A controlled family study of children with DSM-IV bipolar-I disorder and psychiatric co-morbidity.  Psychol Med 2010; 40:1079–1088
[CrossRef] | [PubMed]
 
Nosarti  C;  Reichenberg  A;  Murray  RM;  Cnattingius  S;  Lambe  MP;  Yin  L;  MacCabe  J;  Rifkin  L;  Hultman  CM:  Preterm birth and psychiatric disorders in young adult life.  Arch Gen Psychiatry 2012; 69:E1–E8
[PubMed]
 
Rogers  JM:  Tobacco and pregnancy.  Reprod Toxicol 2009; 28:152–160
[CrossRef] | [PubMed]
 
Miwa  JM;  Freedman  R;  Lester  HA:  Neural systems governed by nicotinic acetylcholine receptors: emerging hypotheses.  Neuron 2011; 70:20–33
[CrossRef] | [PubMed]
 
Mansvelder  HD;  McGehee  DS:  Long-term potentiation of excitatory inputs to brain reward areas by nicotine.  Neuron 2000; 27:349–357
[CrossRef] | [PubMed]
 
Suter  M;  Ma  J;  Harris  AS;  Patterson  L;  Brown  KA;  Shope  C;  Showalter  L;  Abramovici  A;  Aagaard-Tillery  KM:  Maternal tobacco use modestly alters correlated epigenome-wide placental DNA methylation and gene expression.  Epigenetics 2011; 6:1284–1294
[CrossRef] | [PubMed]
 
Leonard  S;  Gault  J;  Hopkins  J;  Logel  J;  Vianzon  R;  Short  M;  Drebing  C;  Berger  R;  Venn  D;  Sirota  P;  Zerbe  G;  Olincy  A;  Ross  RG;  Adler  LE;  Freedman  R:  Association of promoter variants in the alpha7 nicotinic acetylcholine receptor subunit gene with an inhibitory deficit found in schizophrenia.  Arch Gen Psychiatry 2002; 59:1085–1096
[CrossRef] | [PubMed]
 
Martin  LF;  Leonard  S;  Hall  MH;  Tregellas  JR;  Freedman  R;  Olincy  A:  Sensory gating and alpha-7 nicotinic receptor gene allelic variants in schizoaffective disorder, bipolar type.  Am J Med Genet B Neuropsychiatr Genet 2007; 144B:611–614
[CrossRef] | [PubMed]
 
Hussain  S;  Kayne  E;  Guwanardane  N;  Petrides  G:  Varenicline induced mania in a 51-year-old patient without history of bipolar illness.  Prog Neuropsychopharmacol Biol Psychiatry 2011; 35:1162–1163
[CrossRef] | [PubMed]
 
Ernst  M;  Moolchan  ET;  Robinson  ML:  Behavioral and neural consequences of prenatal exposure to nicotine.  J Am Acad Child Adolesc Psychiatry 2001; 40:630–641
[CrossRef] | [PubMed]
 
Fowles  J;  Dybing  E:  Application of toxicological risk assessment principles to the chemical constituents of cigarette smoke.  Tob Control 2003; 12:424–430
[CrossRef] | [PubMed]
 
Boyd  NR;  Windsor  RA;  Perkins  LL;  Lowe  JB:  Quality of measurement of smoking status by self-report and saliva cotinine among pregnant women.  Matern Child Health J 1998; 2:77–83
[CrossRef] | [PubMed]
 
D'Onofrio  BM;  Van Hulle  CA;  Goodnight  JA;  Rathouz  PJ;  Lahey  BB:  Is maternal smoking during pregnancy a causal environmental risk factor for adolescent antisocial behavior? testing etiological theories and assumptions.  Psychol Med 2012; 42:1535–1545
[CrossRef] | [PubMed]
 
Ellingson  JM;  Rickert  ME;  Lichtenstein  P;  Langstrom  N;  D'Onofrio  BM:  Disentangling the relationships between maternal smoking during pregnancy and co-occurring risk factors.  Psychol Med 2012; 42:1547–1557
[CrossRef] | [PubMed]
 
Thapar  A;  Rutter  M:  Do prenatal risk factors cause psychiatric disorder? be wary of causal claims.  Br J Psychiatry 2009; 195:100–101
[CrossRef] | [PubMed]
 
Chapman  S;  Freeman  B:  Markers of the denormalisation of smoking and the tobacco industry.  Tob Control 2008; 17:25–31
[CrossRef] | [PubMed]
 
References Container
+
+

CME Activity

There is currently no quiz available for this resource. Please click here to go to the CME page to find another.
Submit a Comments
Please read the other comments before you post yours. Contributors must reveal any conflict of interest.
Comments are moderated and will appear on the site at the discertion of APA editorial staff.

* = Required Field
(if multiple authors, separate names by comma)
Example: John Doe



Related Content
See Also...
Books
Dulcan's Textbook of Child and Adolescent Psychiatry > Chapter 16.  >
DSM-5™ Clinical Cases > Chapter 3.  >
Manual of Clinical Psychopharmacology, 7th Edition > Chapter 5.  >
The American Psychiatric Publishing Textbook of Psychopharmacology, 4th Edition > Chapter 64.  >
The American Psychiatric Publishing Textbook of Psychopharmacology, 4th Edition > Chapter 44.  >
Topic Collections
Psychiatric News
APA Guidelines
PubMed Articles