Maternal Infection during Pregnancy and Attention-Deficit Hyperactivity Disorder in Children: A Systematic Review and Meta-Analysis
Abstract
Background: We aimed to determine the association between maternal infections during pregnancy with risk of Attention-Deficit Hyperactivity Disorder (ADHD) in children.
Methods: A systematic literature search was performed utilizing the online databases PubMed, Scopus, and Web of Sciences up to July 2020. Random-effects meta-analyses were applied to estimate pooled relative risk (RR). Heterogeneity, study quality and publication bias were assessed through I2 value, Newcastle–Ottawa scale (NOS) and Egger's test, respectively.
Results: Thirteen articles involving 1401904 mother-child pairs were included. The result of meta-analysis showed that the risk of ADHD increased by 30% among children whose mothers took any infections during pregnancy (pooled RR=1.30, 95% CI: 1.14-1.49; I2=85.5, P<0.001). Overall, the included studies were good in quality and no publication bias was found (P=0.23, Egger’s test).
Conclusion: Maternal infections during pregnancy might be associated with an increased risk of ADHD in children.
1. Faraone SV, Sergeant J, Gillberg C, et al (2003). The worldwide prevalence of ADHD: is it an American condition? World J Psychiatry, 2(2):104-13.
2. Thomas R, Sanders S, Doust J, et al (2015). Prevalence of attention-deficit/hyperactivity disorder: a systematic review and meta-analysis. Pediatrics, 135(4): e994–e1001.
3. Bruchmuller K, Margraf J, Schneider S (2012). Is ADHD diagnosed in accord with diagnostic criteria? Overdiagnosis and influence of client gender on diagnosis. Consult Clin Psychol, 80(1):128-38.
4. Cuffe SP, Moore CG, McKeown RE (2005). Prevalence and correlates of ADHD symptoms in the national health interview survey. J Atten Disord, 9(2):392-401.
5. Biederman J, Petty CR, Monuteaux MC, et al (2010). Adult psychiatric outcomes of girls with attention deficit hyperactivity disorder: 11-year follow-up in a longitudinal case-control study. Am J Psychiatry, 167(4):409-17.
6. Grazioli VS, Gmel G, Rougemont-Bucking A, et al (2019). Attention deficit hyperactivity disorder and future alcohol outcomes: Examining the roles of coping and enhancement drinking motives among young men. PloS One, 14(6): e0218469.
7. McGough JJ, Smalley SL, McCracken JT, et al (2005). Psychiatric comorbidity in adult attention deficit hyperactivity disorder: findings from multiplex families. Am J Psychiatry, 162(9):1621-7.
8. Baldessarini RJ, Tondo L, Pinna M, et al (2019). Suicidal risk factors in major affective disorders. Br J Psychiatry, 1-6.
9. Das D, Cherbuin N, Butterworth P, et al (2012). A population-based study of attention deficit/hyperactivity disorder symptoms and associated impairment in middle-aged adults. PloS One, 7(2):e31500.
10. Mpango RS, Kinyanda E, Rukundo GZ, et al (2017). Prevalence and correlates for ADHD and relation with social and academic functioning among children and adolescents with HIV/AIDS in Uganda. BMC Psychiatry, 17(1):336.
11. Chen VC, Chan HL, Wu SI , et al (2019). Attention-Deficit/Hyperactivity Disorder and Mortality Risk in Taiwan. JAMA Netw Open, 2(8):e198714.
12. Faraone SV, Perlis RH, Doyle AE, et al (2005). Molecular genetics of attention-deficit/hyperactivity disorder. Biol Psychiatry, 57(11):1313-23.
13. Hayman V, Fernandez TV (2018). Genetic Insights Into ADHD Biology. Front Psychol, 9:251.
14. Russell AE, Ford T, Williams R, et al (2016). The Association Between Socioeconomic Disadvantage and Attention Deficit/Hyperactivity Disorder (ADHD): A Systematic Review. Child Psychiatry Hum Dev, 47(3):440-58.
15. Lee MJ, Chou MC, Chou WJ, et al (2018). Heavy Metals' Effect on Susceptibility to Attention-Deficit/Hyperactivity Disorder: Implication of Lead, Cadmium, and Antimony. Int J Environ Res, 15(6):1221.
16. Silva D, Colvin L, Hagemann E, et al (2014). Environmental risk factors by gender associated with attention-deficit/hyperactivity disorder. Pediatrics, 133(1): e14–e22.
17. Mick E, Biederman J, Prince J, et al (2002). Impact of low birth weight on attention-deficit hyperactivity disorder. J Dev Behav Pediatr, 23(1):16-22.
18. Dong T, Hu W, Zhou X, et al (2018). Prenatal exposure to maternal smoking during pregnancy and attention-deficit/hyperactivity disorder in offspring: A meta-analysis. Reprod Toxicol, 76:63-70.
19. Huang L, Wang Y, Zhang L, et al (2018). Maternal Smoking and Attention-Deficit/Hyperactivity Disorder in Offspring: A Meta-analysis. Pediatrics, 141(1): e20172465
20. Pagnin D, Zamboni Grecco ML, Furtado EF (2019). Prenatal alcohol use as a risk for attention-deficit/hyperactivity disorder. Eur Arch Psychiatry Clin Neurosci, 269(6):681-7.
21. Mann JR, McDermott S (2011). Are maternal genitourinary infection and pre-eclampsia associated with ADHD in school-aged children? J Atten Disord, 15(8):667-73.
22. Werenberg Dreier J, Nybo Andersen AM, Hvolby A, et al (2016). Fever and infections in pregnancy and risk of attention deficit/hyperactivity disorder in the offspring. J Child Psychol, 57(4):540-8.
23. Ystrom E, Gustavson K, Brandlistuen RE, et al (2017). Prenatal Exposure to Acetaminophen and Risk of ADHD. Pediatrics, 140(5):e20163840.
24. Atladottir HO, Thorsen P, Ostergaard L, et al (2010). Maternal infection requiring hospitalization during pregnancy and autism spectrum disorders. J Autism Dev Disord, 40(12):1423-30.
25. Blomstrom A, Karlsson H, Gardner R, et al (2016). Associations Between Maternal Infection During Pregnancy, Childhood Infections, and the Risk of Subsequent Psychotic Disorder--A Swedish Cohort Study of Nearly 2 Million Individuals. Schizophr Bull, 42(1):125-33.
26. Khandaker GM, Cousins L, Deakin J, et al (2015). Inflammation and immunity in schizophrenia: implications for pathophysiology and treatment. The lancet Psychiatry, 2015;2(3):258-70.
27. Moher D, Shamseer L, Clarke M, et al (2015). Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev, 4:1.
28. Wells GA, Shea B, O'Connell D, et al (2019). The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Accessed September [Available from: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp
29. Modesti PA, Reboldi G, Cappuccio FP, et al (2016). Panethnic Differences in Blood Pressure in Europe: A Systematic Review and Meta-Analysis. PloS One, 11(1):e0147601.
30. Cummings P (2009). The relative merits of risk ratios and odds ratios. Arch Pediatr Adolesc Med, 163(5):438-45.
31. Bilenberg N, Hougaard D, Norgaard-Pedersen B, et al (2011). Twin study on transplacental-acquired antibodies and attention deficit/hyperactivity disorder--A pilot study. J Neuroimmunol, 236(1-2):72-5.
32. Liew Z, Ritz B, Rebordosa C, et al (2014). Acetaminophen use during pregnancy, behavioral problems, and hyperkinetic disorders. JAMA Pediatrics, 168(4):313-20.
33. Wiggs KK, Rickert ME, Hernandez-Diaz S, et al (2017). A Family-Based Study of the Association Between Labor Induction and Offspring Attention-Deficit Hyperactivity Disorder and Low Academic Achievement. Behav Genet, 47(4):383-93.
34. Afsharpaiman S, Khosravi MH, Faridchehr M, et al (2016). Assessment of Toxoplasma Seropositivity in Children Suffering from Attention Deficit Hyperactivity Disorder. Galen Med J, 5(4):188-93.
35. Arpino C, Marzio M, D'Argenzio L, et al (2005). Exanthematic diseases during pregnancy and attention-deficit/hyperactivity disorder (ADHD). Eur J Paediatr Neurol, 9(5):363-5.
36. Chudal R, Brown AS, Gyllenberg D, et al (2020). Maternal serum C-reactive protein (CRP) and offspring attention deficit hyperactivity disorder (ADHD). Eur Child Adolesc, 29(2):239-247.
37. Downey LC, O'Shea TM, Allred EN, et al (2015). Antenatal and early postnatal antecedents of parent-reported attention problems at 2 years of age. J Pediatr, 166(1):20-5.e1.
38. Ginsberg Y, D'Onofrio BM, Rickert ME, et al (2019). Maternal infection requiring hospitalization during pregnancy and attention-deficit hyperactivity disorder in offspring: a quasi-experimental family-based study. J Child Psychol Psychiatry, 60(2):160-8.
39. Gustavson K, Ask H, Ystrom E, et al (2019). Maternal fever during pregnancy and offspring attention deficit hyperactivity disorder. Sci Rep, 9(1):9519.
40. Mellins CA, Brackis-Cott E, Leu CS, et al (2009). Rates and types of psychiatric disorders in perinatally human immunodeficiency virus-infected youth and seroreverters. J Child Psychol Psychiatry, 50(9):1131-8.
41. Oerlemans AM, Burmanje MJ, Franke B, et al (2016). Identifying Unique Versus Shared Pre- and Perinatal Risk Factors for ASD and ADHD Using a Simplex-Multiplex Stratification. J Abnorm Child Psychol, 44(5):923-35.
42. Pineda DA, Palacio LG, Puerta IC, et al (2007). Environmental influences that affect attention deficit/hyperactivity disorder: study of a genetic isolate. Eur Child Adolesc Psychiatry, 16(5):337-46.
43. Schmitt J, Romanos M (2012). Prenatal and perinatal risk factors for attention-deficit/hyperactivity disorder. Arch Pediatr Adolesc Med, 166(11):1074-5.
44. Jiang HY, Xu LL, Shao L, et al (2016). Maternal infection during pregnancy and risk of autism spectrum disorders: A systematic review and meta-analysis. Brain Behav Immun, 58:165-72.
45. Scola G, Duong A (2017). Prenatal maternal immune activation and brain development with relevance to psychiatric disorders. Neuroscience, 346:403-8.
46. Schultz R, Read AW, Straton JA, et al (1991). Genitourinary tract infections in pregnancy and low birth weight: case-control study in Australian aboriginal women. BMJ, 303(6814):1369-73.
47. Franz AP, Bolat GU, Bolat H, et al (2018). Attention-Deficit/Hyperactivity Disorder and Very Preterm/Very Low Birth Weight: A Meta-analysis. Pediatrics, 141(1): e20171645.
48. Yue Y, Tang Y, Tang J, et al (2018). Maternal infection during pregnancy and type 1 diabetes mellitus in offspring: a systematic review and meta-analysis. Epidemiol Infect, 146(16):2131-8.
49. Ye Z, Wang L, Yang T, et al (2019). Maternal Viral Infection and Risk of Fetal Congenital Heart Diseases: A Meta-Analysis of Observational Studies. J Am Heart Assoc, 8(9):e011264.
50. He J, Liu ZW, Lu YP, et al (2017). A Systematic Review and Meta-Analysis of Influenza A Virus Infection During Pregnancy Associated with an Increased Risk for Stillbirth and Low Birth Weight. Kidney Blood Press Res, 42(2):232-43.
2. Thomas R, Sanders S, Doust J, et al (2015). Prevalence of attention-deficit/hyperactivity disorder: a systematic review and meta-analysis. Pediatrics, 135(4): e994–e1001.
3. Bruchmuller K, Margraf J, Schneider S (2012). Is ADHD diagnosed in accord with diagnostic criteria? Overdiagnosis and influence of client gender on diagnosis. Consult Clin Psychol, 80(1):128-38.
4. Cuffe SP, Moore CG, McKeown RE (2005). Prevalence and correlates of ADHD symptoms in the national health interview survey. J Atten Disord, 9(2):392-401.
5. Biederman J, Petty CR, Monuteaux MC, et al (2010). Adult psychiatric outcomes of girls with attention deficit hyperactivity disorder: 11-year follow-up in a longitudinal case-control study. Am J Psychiatry, 167(4):409-17.
6. Grazioli VS, Gmel G, Rougemont-Bucking A, et al (2019). Attention deficit hyperactivity disorder and future alcohol outcomes: Examining the roles of coping and enhancement drinking motives among young men. PloS One, 14(6): e0218469.
7. McGough JJ, Smalley SL, McCracken JT, et al (2005). Psychiatric comorbidity in adult attention deficit hyperactivity disorder: findings from multiplex families. Am J Psychiatry, 162(9):1621-7.
8. Baldessarini RJ, Tondo L, Pinna M, et al (2019). Suicidal risk factors in major affective disorders. Br J Psychiatry, 1-6.
9. Das D, Cherbuin N, Butterworth P, et al (2012). A population-based study of attention deficit/hyperactivity disorder symptoms and associated impairment in middle-aged adults. PloS One, 7(2):e31500.
10. Mpango RS, Kinyanda E, Rukundo GZ, et al (2017). Prevalence and correlates for ADHD and relation with social and academic functioning among children and adolescents with HIV/AIDS in Uganda. BMC Psychiatry, 17(1):336.
11. Chen VC, Chan HL, Wu SI , et al (2019). Attention-Deficit/Hyperactivity Disorder and Mortality Risk in Taiwan. JAMA Netw Open, 2(8):e198714.
12. Faraone SV, Perlis RH, Doyle AE, et al (2005). Molecular genetics of attention-deficit/hyperactivity disorder. Biol Psychiatry, 57(11):1313-23.
13. Hayman V, Fernandez TV (2018). Genetic Insights Into ADHD Biology. Front Psychol, 9:251.
14. Russell AE, Ford T, Williams R, et al (2016). The Association Between Socioeconomic Disadvantage and Attention Deficit/Hyperactivity Disorder (ADHD): A Systematic Review. Child Psychiatry Hum Dev, 47(3):440-58.
15. Lee MJ, Chou MC, Chou WJ, et al (2018). Heavy Metals' Effect on Susceptibility to Attention-Deficit/Hyperactivity Disorder: Implication of Lead, Cadmium, and Antimony. Int J Environ Res, 15(6):1221.
16. Silva D, Colvin L, Hagemann E, et al (2014). Environmental risk factors by gender associated with attention-deficit/hyperactivity disorder. Pediatrics, 133(1): e14–e22.
17. Mick E, Biederman J, Prince J, et al (2002). Impact of low birth weight on attention-deficit hyperactivity disorder. J Dev Behav Pediatr, 23(1):16-22.
18. Dong T, Hu W, Zhou X, et al (2018). Prenatal exposure to maternal smoking during pregnancy and attention-deficit/hyperactivity disorder in offspring: A meta-analysis. Reprod Toxicol, 76:63-70.
19. Huang L, Wang Y, Zhang L, et al (2018). Maternal Smoking and Attention-Deficit/Hyperactivity Disorder in Offspring: A Meta-analysis. Pediatrics, 141(1): e20172465
20. Pagnin D, Zamboni Grecco ML, Furtado EF (2019). Prenatal alcohol use as a risk for attention-deficit/hyperactivity disorder. Eur Arch Psychiatry Clin Neurosci, 269(6):681-7.
21. Mann JR, McDermott S (2011). Are maternal genitourinary infection and pre-eclampsia associated with ADHD in school-aged children? J Atten Disord, 15(8):667-73.
22. Werenberg Dreier J, Nybo Andersen AM, Hvolby A, et al (2016). Fever and infections in pregnancy and risk of attention deficit/hyperactivity disorder in the offspring. J Child Psychol, 57(4):540-8.
23. Ystrom E, Gustavson K, Brandlistuen RE, et al (2017). Prenatal Exposure to Acetaminophen and Risk of ADHD. Pediatrics, 140(5):e20163840.
24. Atladottir HO, Thorsen P, Ostergaard L, et al (2010). Maternal infection requiring hospitalization during pregnancy and autism spectrum disorders. J Autism Dev Disord, 40(12):1423-30.
25. Blomstrom A, Karlsson H, Gardner R, et al (2016). Associations Between Maternal Infection During Pregnancy, Childhood Infections, and the Risk of Subsequent Psychotic Disorder--A Swedish Cohort Study of Nearly 2 Million Individuals. Schizophr Bull, 42(1):125-33.
26. Khandaker GM, Cousins L, Deakin J, et al (2015). Inflammation and immunity in schizophrenia: implications for pathophysiology and treatment. The lancet Psychiatry, 2015;2(3):258-70.
27. Moher D, Shamseer L, Clarke M, et al (2015). Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev, 4:1.
28. Wells GA, Shea B, O'Connell D, et al (2019). The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Accessed September [Available from: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp
29. Modesti PA, Reboldi G, Cappuccio FP, et al (2016). Panethnic Differences in Blood Pressure in Europe: A Systematic Review and Meta-Analysis. PloS One, 11(1):e0147601.
30. Cummings P (2009). The relative merits of risk ratios and odds ratios. Arch Pediatr Adolesc Med, 163(5):438-45.
31. Bilenberg N, Hougaard D, Norgaard-Pedersen B, et al (2011). Twin study on transplacental-acquired antibodies and attention deficit/hyperactivity disorder--A pilot study. J Neuroimmunol, 236(1-2):72-5.
32. Liew Z, Ritz B, Rebordosa C, et al (2014). Acetaminophen use during pregnancy, behavioral problems, and hyperkinetic disorders. JAMA Pediatrics, 168(4):313-20.
33. Wiggs KK, Rickert ME, Hernandez-Diaz S, et al (2017). A Family-Based Study of the Association Between Labor Induction and Offspring Attention-Deficit Hyperactivity Disorder and Low Academic Achievement. Behav Genet, 47(4):383-93.
34. Afsharpaiman S, Khosravi MH, Faridchehr M, et al (2016). Assessment of Toxoplasma Seropositivity in Children Suffering from Attention Deficit Hyperactivity Disorder. Galen Med J, 5(4):188-93.
35. Arpino C, Marzio M, D'Argenzio L, et al (2005). Exanthematic diseases during pregnancy and attention-deficit/hyperactivity disorder (ADHD). Eur J Paediatr Neurol, 9(5):363-5.
36. Chudal R, Brown AS, Gyllenberg D, et al (2020). Maternal serum C-reactive protein (CRP) and offspring attention deficit hyperactivity disorder (ADHD). Eur Child Adolesc, 29(2):239-247.
37. Downey LC, O'Shea TM, Allred EN, et al (2015). Antenatal and early postnatal antecedents of parent-reported attention problems at 2 years of age. J Pediatr, 166(1):20-5.e1.
38. Ginsberg Y, D'Onofrio BM, Rickert ME, et al (2019). Maternal infection requiring hospitalization during pregnancy and attention-deficit hyperactivity disorder in offspring: a quasi-experimental family-based study. J Child Psychol Psychiatry, 60(2):160-8.
39. Gustavson K, Ask H, Ystrom E, et al (2019). Maternal fever during pregnancy and offspring attention deficit hyperactivity disorder. Sci Rep, 9(1):9519.
40. Mellins CA, Brackis-Cott E, Leu CS, et al (2009). Rates and types of psychiatric disorders in perinatally human immunodeficiency virus-infected youth and seroreverters. J Child Psychol Psychiatry, 50(9):1131-8.
41. Oerlemans AM, Burmanje MJ, Franke B, et al (2016). Identifying Unique Versus Shared Pre- and Perinatal Risk Factors for ASD and ADHD Using a Simplex-Multiplex Stratification. J Abnorm Child Psychol, 44(5):923-35.
42. Pineda DA, Palacio LG, Puerta IC, et al (2007). Environmental influences that affect attention deficit/hyperactivity disorder: study of a genetic isolate. Eur Child Adolesc Psychiatry, 16(5):337-46.
43. Schmitt J, Romanos M (2012). Prenatal and perinatal risk factors for attention-deficit/hyperactivity disorder. Arch Pediatr Adolesc Med, 166(11):1074-5.
44. Jiang HY, Xu LL, Shao L, et al (2016). Maternal infection during pregnancy and risk of autism spectrum disorders: A systematic review and meta-analysis. Brain Behav Immun, 58:165-72.
45. Scola G, Duong A (2017). Prenatal maternal immune activation and brain development with relevance to psychiatric disorders. Neuroscience, 346:403-8.
46. Schultz R, Read AW, Straton JA, et al (1991). Genitourinary tract infections in pregnancy and low birth weight: case-control study in Australian aboriginal women. BMJ, 303(6814):1369-73.
47. Franz AP, Bolat GU, Bolat H, et al (2018). Attention-Deficit/Hyperactivity Disorder and Very Preterm/Very Low Birth Weight: A Meta-analysis. Pediatrics, 141(1): e20171645.
48. Yue Y, Tang Y, Tang J, et al (2018). Maternal infection during pregnancy and type 1 diabetes mellitus in offspring: a systematic review and meta-analysis. Epidemiol Infect, 146(16):2131-8.
49. Ye Z, Wang L, Yang T, et al (2019). Maternal Viral Infection and Risk of Fetal Congenital Heart Diseases: A Meta-Analysis of Observational Studies. J Am Heart Assoc, 8(9):e011264.
50. He J, Liu ZW, Lu YP, et al (2017). A Systematic Review and Meta-Analysis of Influenza A Virus Infection During Pregnancy Associated with an Increased Risk for Stillbirth and Low Birth Weight. Kidney Blood Press Res, 42(2):232-43.
| Files | ||
| Issue | Vol 51 No 12 (2022) | |
| Section | Review Article(s) | |
| DOI | https://doi.org/10.18502/ijph.v51i12.11458 | |
| Keywords | ||
| Maternal infection Pregnancy Disorder Hyperactivity | ||
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How to Cite
1.
Ayubi E, Mansori K. Maternal Infection during Pregnancy and Attention-Deficit Hyperactivity Disorder in Children: A Systematic Review and Meta-Analysis. Iran J Public Health. 2022;51(12):2674-2687.
