Skip to main content
Top
Published in: BMC Pediatrics 1/2014

Open Access 01-12-2014 | Research article

Birth after preeclamptic pregnancies: association with allergic sensitization and allergic rhinoconjunctivitis in late childhood; a historically matched cohort study

Authors: Kristine Kjer Byberg, Bjorn Ogland, Geir Egil Eide, Knut Øymar

Published in: BMC Pediatrics | Issue 1/2014

Login to get access

Abstract

Background

The development of allergic sensitization and allergic disease may be related to factors during intrauterine life, but the role of maternal preeclampsia is not known.
We studied if maternal preeclampsia is associated with long-term allergic sensitization, allergic rhinoconjunctivitis, atopic dermatitis, asthma and with altered lung function in late childhood.

Methods

617 children participated in a 1:2 matched and controlled historical cohort study; 230 born after preeclamptic pregnancies and 387 born after normotensive pregnancies. Specific IgE in serum and lung function were measured at the age of 12.8 years and questionnaires on maternal and adolescent data were completed at the ages of 10.8 years (girls) and 11.8 years (boys), and at 12.8 years (both genders). The association between birth after preeclampsia and the main outcome measures allergic sensitization, allergic rhinoconjunctivitis, atopic dermatitis, asthma and lung function in late childhood were analysed with multiple regression analyses, including possible confounders.

Results

Severe maternal preeclampsia was associated with high level allergic sensitization (sum of specific IgE in serum ≥ 3.9 kU/l; the 25 percentile for all children being sensitized); odds ratio (OR): 3.79; 95% confidence interval (CI): (1.54, 9.32); p = 0.015 and with allergic rhinoconjunctivitis in offspring; OR: 2.22, 95% CI: (1.19, 4.14), p = 0.047. Preeclampsia was not associated with atopic dermatitis, asthma or altered lung function in late childhood.

Conclusion

Maternal preeclampsia was associated with allergic sensitization and allergic rhinoconjunctivitis in offspring in late childhood, but not with other atopic diseases.
Appendix
Available only for authorised users
Literature
1.
go back to reference Schernhammer ES, Vutuc C, Waldhor T, Haidinger G: Time trends of the prevalence of asthma and allergic disease in Austrian children. Pediatr Allergy Immunol. 2008, 19 (2): 125-131. 10.1111/j.1399-3038.2007.00597.x.CrossRefPubMed Schernhammer ES, Vutuc C, Waldhor T, Haidinger G: Time trends of the prevalence of asthma and allergic disease in Austrian children. Pediatr Allergy Immunol. 2008, 19 (2): 125-131. 10.1111/j.1399-3038.2007.00597.x.CrossRefPubMed
2.
go back to reference de Boo HA, Harding JE: The developmental origins of adult disease (Barker) hypothesis. Aust N Z J Obstet Gynaecol. 2006, 46 (1): 4-14. 10.1111/j.1479-828X.2006.00506.x.CrossRefPubMed de Boo HA, Harding JE: The developmental origins of adult disease (Barker) hypothesis. Aust N Z J Obstet Gynaecol. 2006, 46 (1): 4-14. 10.1111/j.1479-828X.2006.00506.x.CrossRefPubMed
3.
go back to reference De Luca G, Olivieri F, Melotti G, Aiello G, Lubrano L, Boner AL: Fetal and early postnatal life roots of asthma. J Matern Fetal Neonatal Med. 2010, 23 (Suppl 3): 80-83.CrossRefPubMed De Luca G, Olivieri F, Melotti G, Aiello G, Lubrano L, Boner AL: Fetal and early postnatal life roots of asthma. J Matern Fetal Neonatal Med. 2010, 23 (Suppl 3): 80-83.CrossRefPubMed
4.
go back to reference Diesner SC, Forster-Waldl E, Olivera A, Pollak A, Jensen-Jarolim E, Untersmayr E: Perspectives on immunomodulation early in life. Pediatr Allergy Immunol. 2012, 23 (3): 210-223. 10.1111/j.1399-3038.2011.01259.x.CrossRefPubMed Diesner SC, Forster-Waldl E, Olivera A, Pollak A, Jensen-Jarolim E, Untersmayr E: Perspectives on immunomodulation early in life. Pediatr Allergy Immunol. 2012, 23 (3): 210-223. 10.1111/j.1399-3038.2011.01259.x.CrossRefPubMed
6.
go back to reference Herberth G, Hinz D, Roder S, Schlink U, Sack U, Diez U, Borte M, Lehmann I: Maternal immune status in pregnancy is related to offspring’s immune responses and atopy risk. Allergy. 2011, 66 (8): 1065-1074. 10.1111/j.1398-9995.2011.02587.x.CrossRefPubMed Herberth G, Hinz D, Roder S, Schlink U, Sack U, Diez U, Borte M, Lehmann I: Maternal immune status in pregnancy is related to offspring’s immune responses and atopy risk. Allergy. 2011, 66 (8): 1065-1074. 10.1111/j.1398-9995.2011.02587.x.CrossRefPubMed
7.
go back to reference Pfefferle P, Bocking C, Renz H: Maternal cytokine profiles during pregnancy - predictors for later allergy or just reading the tea leaves?. Allergy. 2011, 66 (8): 987-988. 10.1111/j.1398-9995.2011.02665.x.CrossRefPubMed Pfefferle P, Bocking C, Renz H: Maternal cytokine profiles during pregnancy - predictors for later allergy or just reading the tea leaves?. Allergy. 2011, 66 (8): 987-988. 10.1111/j.1398-9995.2011.02665.x.CrossRefPubMed
9.
go back to reference Jim B, Sharma S, Kebede T, Acharya A: Hypertension in pregnancy: a comprehensive update. Cardiol Rev. 2010, 18 (4): 178-189. 10.1097/CRD.0b013e3181c60ca6.CrossRefPubMed Jim B, Sharma S, Kebede T, Acharya A: Hypertension in pregnancy: a comprehensive update. Cardiol Rev. 2010, 18 (4): 178-189. 10.1097/CRD.0b013e3181c60ca6.CrossRefPubMed
10.
go back to reference Szarka A, Rigo J, Lazar L, Beko G, Molvarec A: Circulating cytokines, chemokines and adhesion molecules in normal pregnancy and preeclampsia determined by multiplex suspension array. BMC Immunol. 2010, 11: 59-10.1186/1471-2172-11-59.CrossRefPubMedPubMedCentral Szarka A, Rigo J, Lazar L, Beko G, Molvarec A: Circulating cytokines, chemokines and adhesion molecules in normal pregnancy and preeclampsia determined by multiplex suspension array. BMC Immunol. 2010, 11: 59-10.1186/1471-2172-11-59.CrossRefPubMedPubMedCentral
11.
go back to reference Nafstad P, Magnus P, Jaakkola JJ: Risk of childhood asthma and allergic rhinitis in relation to pregnancy complications. J Allergy Clin Immunol. 2000, 106 (5): 867-873. 10.1067/mai.2000.110558.CrossRefPubMed Nafstad P, Magnus P, Jaakkola JJ: Risk of childhood asthma and allergic rhinitis in relation to pregnancy complications. J Allergy Clin Immunol. 2000, 106 (5): 867-873. 10.1067/mai.2000.110558.CrossRefPubMed
12.
go back to reference Nafstad P, Samuelsen SO, Irgens LM, Bjerkedal T: Pregnancy complications and the risk of asthma among Norwegians born between 1967 and 1993. Eur J Epidemiol. 2003, 18 (8): 755-761.CrossRefPubMed Nafstad P, Samuelsen SO, Irgens LM, Bjerkedal T: Pregnancy complications and the risk of asthma among Norwegians born between 1967 and 1993. Eur J Epidemiol. 2003, 18 (8): 755-761.CrossRefPubMed
13.
go back to reference Keski-Nisula L, Heinonen S, Remes S, Pekkanen J: Pre-eclampsia, placental abruption and increased risk of atopic sensitization in male adolescent offspring. Am J Reprod Immunol. 2009, 62 (5): 293-300. 10.1111/j.1600-0897.2009.00738.x.CrossRefPubMed Keski-Nisula L, Heinonen S, Remes S, Pekkanen J: Pre-eclampsia, placental abruption and increased risk of atopic sensitization in male adolescent offspring. Am J Reprod Immunol. 2009, 62 (5): 293-300. 10.1111/j.1600-0897.2009.00738.x.CrossRefPubMed
14.
go back to reference Gagliardi L, Rusconi F, Da Fre M, Mello G, Carnielli V, Di Lallo D, Macagno F, Miniaci S, Corchia C, Cuttini M: Pregnancy disorders leading to very preterm birth influence neonatal outcomes: results of the population-based ACTION cohort study. Pediatr Res. 2013, 73 (6): 794-801. 10.1038/pr.2013.52.CrossRefPubMed Gagliardi L, Rusconi F, Da Fre M, Mello G, Carnielli V, Di Lallo D, Macagno F, Miniaci S, Corchia C, Cuttini M: Pregnancy disorders leading to very preterm birth influence neonatal outcomes: results of the population-based ACTION cohort study. Pediatr Res. 2013, 73 (6): 794-801. 10.1038/pr.2013.52.CrossRefPubMed
15.
go back to reference Wang A, Holston AM, Yu KF, Zhang J, Toporsian M, Karumanchi SA, Levine RJ: Circulating anti-angiogenic factors during hypertensive pregnancy and increased risk of respiratory distress syndrome in preterm neonates. J Matern Fetal Neonatal Med. 2011, 25 (8): 1447-1452.CrossRefPubMedPubMedCentral Wang A, Holston AM, Yu KF, Zhang J, Toporsian M, Karumanchi SA, Levine RJ: Circulating anti-angiogenic factors during hypertensive pregnancy and increased risk of respiratory distress syndrome in preterm neonates. J Matern Fetal Neonatal Med. 2011, 25 (8): 1447-1452.CrossRefPubMedPubMedCentral
16.
go back to reference Kotecha SJ, Watkins WJ, Heron J, Henderson J, Dunstan FD, Kotecha S: Spirometric lung function in school-age children: effect of intrauterine growth retardation and catch-up growth. Am J Respir Crit Care Med. 2010, 181 (9): 969-974. 10.1164/rccm.200906-0897OC.CrossRefPubMedPubMedCentral Kotecha SJ, Watkins WJ, Heron J, Henderson J, Dunstan FD, Kotecha S: Spirometric lung function in school-age children: effect of intrauterine growth retardation and catch-up growth. Am J Respir Crit Care Med. 2010, 181 (9): 969-974. 10.1164/rccm.200906-0897OC.CrossRefPubMedPubMedCentral
17.
go back to reference Ogland B, Vatten LJ, Romundstad PR, Nilsen ST, Forman MR: Pubertal anthropometry in sons and daughters of women with preeclamptic or normotensive pregnancies. Arch Dis Child. 2009, 94 (11): 855-859. 10.1136/adc.2008.150870.CrossRefPubMed Ogland B, Vatten LJ, Romundstad PR, Nilsen ST, Forman MR: Pubertal anthropometry in sons and daughters of women with preeclamptic or normotensive pregnancies. Arch Dis Child. 2009, 94 (11): 855-859. 10.1136/adc.2008.150870.CrossRefPubMed
18.
go back to reference Marsal K, Persson PH, Larsen T, Lilja H, Selbing A, Sultan B: Intrauterine growth curves based on ultrasonically estimated foetal weights. Acta Paediatr. 1996, 85 (7): 843-848. 10.1111/j.1651-2227.1996.tb14164.x.CrossRefPubMed Marsal K, Persson PH, Larsen T, Lilja H, Selbing A, Sultan B: Intrauterine growth curves based on ultrasonically estimated foetal weights. Acta Paediatr. 1996, 85 (7): 843-848. 10.1111/j.1651-2227.1996.tb14164.x.CrossRefPubMed
19.
go back to reference Juliusson PB, Roelants M, Eide GE, Moster D, Juul A, Hauspie R, Waaler PE, Bjerknes R: Growth references for Norwegian children. Tidsskr Nor Laegeforen. 2009, 129 (4): 281-286.CrossRefPubMed Juliusson PB, Roelants M, Eide GE, Moster D, Juul A, Hauspie R, Waaler PE, Bjerknes R: Growth references for Norwegian children. Tidsskr Nor Laegeforen. 2009, 129 (4): 281-286.CrossRefPubMed
20.
go back to reference Worldwide variation in prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and atopic eczema: ISAAC. The International Study of Asthma and Allergies in Childhood (ISAAC) Steering Committee. Lancet. 1998, 351 (9111): 1225-1232. 10.1016/S0140-6736(97)07302-9. Worldwide variation in prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and atopic eczema: ISAAC. The International Study of Asthma and Allergies in Childhood (ISAAC) Steering Committee. Lancet. 1998, 351 (9111): 1225-1232. 10.1016/S0140-6736(97)07302-9.
21.
go back to reference Quanjer PH, Borsboom GJ, Brunekreef B, Zach M, Forche G, Cotes JE, Sanchis J, Paoletti P: Spirometric reference values for white European children and adolescents: Polgar revisited. Pediatr Pulmonol. 1995, 19 (2): 135-142. 10.1002/ppul.1950190209.CrossRefPubMed Quanjer PH, Borsboom GJ, Brunekreef B, Zach M, Forche G, Cotes JE, Sanchis J, Paoletti P: Spirometric reference values for white European children and adolescents: Polgar revisited. Pediatr Pulmonol. 1995, 19 (2): 135-142. 10.1002/ppul.1950190209.CrossRefPubMed
22.
go back to reference Jonsson Y, Ruber M, Matthiesen L, Berg G, Nieminen K, Sharma S, Ernerudh J, Ekerfelt C: Cytokine mapping of sera from women with preeclampsia and normal pregnancies. J Reprod Immunol. 2006, 70 (1–2): 83-91.CrossRefPubMed Jonsson Y, Ruber M, Matthiesen L, Berg G, Nieminen K, Sharma S, Ernerudh J, Ekerfelt C: Cytokine mapping of sera from women with preeclampsia and normal pregnancies. J Reprod Immunol. 2006, 70 (1–2): 83-91.CrossRefPubMed
23.
go back to reference Molvarec A, Shiozaki A, Ito M, Toldi G, Stenczer B, Szarka A, Nakashima A, Vasarhelyi B, Rigo J, Saito S: Increased prevalence of peripheral blood granulysin-producing cytotoxic T lymphocytes in preeclampsia. J Reprod Immunol. 2011, 91 (1–2): 56-63.CrossRefPubMed Molvarec A, Shiozaki A, Ito M, Toldi G, Stenczer B, Szarka A, Nakashima A, Vasarhelyi B, Rigo J, Saito S: Increased prevalence of peripheral blood granulysin-producing cytotoxic T lymphocytes in preeclampsia. J Reprod Immunol. 2011, 91 (1–2): 56-63.CrossRefPubMed
24.
go back to reference Myatt L, Miodovnik M: Prediction of preeclampsia. Semin Perinatol. 1999, 23 (1): 45-57. 10.1016/S0146-0005(99)80059-7.CrossRefPubMed Myatt L, Miodovnik M: Prediction of preeclampsia. Semin Perinatol. 1999, 23 (1): 45-57. 10.1016/S0146-0005(99)80059-7.CrossRefPubMed
25.
go back to reference Aliyu MH, Salihu HM, Lynch O, Alio AP, Marty PJ: Fetal sex and differential survival in preeclampsia and eclampsia. Arch Gynecol Obstet. 2012, 285 (2): 361-365. 10.1007/s00404-011-1984-9.CrossRefPubMed Aliyu MH, Salihu HM, Lynch O, Alio AP, Marty PJ: Fetal sex and differential survival in preeclampsia and eclampsia. Arch Gynecol Obstet. 2012, 285 (2): 361-365. 10.1007/s00404-011-1984-9.CrossRefPubMed
26.
go back to reference van Gool CJ, Thijs C, Dagnelie PC, Henquet CJ, van Houwelingen AC, Schrander J, Menheere PP, van den Brandt PA: Determinants of neonatal IgE level: parity, maternal age, birth season and perinatal essential fatty acid status in infants of atopic mothers. Allergy. 2004, 59 (9): 961-968. 10.1111/j.1398-9995.2004.00528.x.CrossRefPubMed van Gool CJ, Thijs C, Dagnelie PC, Henquet CJ, van Houwelingen AC, Schrander J, Menheere PP, van den Brandt PA: Determinants of neonatal IgE level: parity, maternal age, birth season and perinatal essential fatty acid status in infants of atopic mothers. Allergy. 2004, 59 (9): 961-968. 10.1111/j.1398-9995.2004.00528.x.CrossRefPubMed
27.
go back to reference Alm B, Goksor E, Thengilsdottir H, Pettersson R, Mollborg P, Norvenius G, Erdes L, Aberg N, Wennergren G: Early protective and risk factors for allergic rhinitis at age 4(1/2) yr. Pediatr Allergy Immunol. 2011, 22 (4): 398-404. 10.1111/j.1399-3038.2011.01153.x.CrossRefPubMedPubMedCentral Alm B, Goksor E, Thengilsdottir H, Pettersson R, Mollborg P, Norvenius G, Erdes L, Aberg N, Wennergren G: Early protective and risk factors for allergic rhinitis at age 4(1/2) yr. Pediatr Allergy Immunol. 2011, 22 (4): 398-404. 10.1111/j.1399-3038.2011.01153.x.CrossRefPubMedPubMedCentral
29.
go back to reference Kusunoki T, Mukaida K, Morimoto T, Sakuma M, Yasumi T, Nishikomori R, Heike T: Birth order effect on childhood food allergy. Pediatr Allergy Immunol. 2012, 23 (3): 250-254. 10.1111/j.1399-3038.2011.01246.x.CrossRefPubMed Kusunoki T, Mukaida K, Morimoto T, Sakuma M, Yasumi T, Nishikomori R, Heike T: Birth order effect on childhood food allergy. Pediatr Allergy Immunol. 2012, 23 (3): 250-254. 10.1111/j.1399-3038.2011.01246.x.CrossRefPubMed
30.
go back to reference Karmaus W, Arshad H, Mattes J: Does the sibling effect have its origin in utero? Investigating birth order, cord blood immunoglobulin E concentration, and allergic sensitization at age 4 years. Am J Epidemiol. 2001, 154 (10): 909-915. 10.1093/aje/154.10.909.CrossRefPubMed Karmaus W, Arshad H, Mattes J: Does the sibling effect have its origin in utero? Investigating birth order, cord blood immunoglobulin E concentration, and allergic sensitization at age 4 years. Am J Epidemiol. 2001, 154 (10): 909-915. 10.1093/aje/154.10.909.CrossRefPubMed
31.
go back to reference Triche EW, Saftlas AF, Belanger K, Leaderer BP, Bracken MB: Association of asthma diagnosis, severity, symptoms, and treatment with risk of preeclampsia. Obstet Gynecol. 2004, 104 (3): 585-593. 10.1097/01.AOG.0000136481.05983.91.CrossRefPubMed Triche EW, Saftlas AF, Belanger K, Leaderer BP, Bracken MB: Association of asthma diagnosis, severity, symptoms, and treatment with risk of preeclampsia. Obstet Gynecol. 2004, 104 (3): 585-593. 10.1097/01.AOG.0000136481.05983.91.CrossRefPubMed
32.
go back to reference Hattevig G, Kjellman B, Bjorksten B: Appearance of IgE antibodies to ingested and inhaled allergens during the first 12 years of life in atopic and non-atopic children. Pediatr Allergy Immu : official publication of the European Society of Pediatric Allergy and Immunology. 1993, 4 (4): 182-186. 10.1111/j.1399-3038.1993.tb00089.x.CrossRef Hattevig G, Kjellman B, Bjorksten B: Appearance of IgE antibodies to ingested and inhaled allergens during the first 12 years of life in atopic and non-atopic children. Pediatr Allergy Immu : official publication of the European Society of Pediatric Allergy and Immunology. 1993, 4 (4): 182-186. 10.1111/j.1399-3038.1993.tb00089.x.CrossRef
33.
go back to reference Annesi-Maesano I, Moreau D, Strachan D: In utero and perinatal complications preceding asthma. Allergy. 2001, 56 (6): 491-497. 10.1034/j.1398-9995.2001.056006491.x.CrossRefPubMed Annesi-Maesano I, Moreau D, Strachan D: In utero and perinatal complications preceding asthma. Allergy. 2001, 56 (6): 491-497. 10.1034/j.1398-9995.2001.056006491.x.CrossRefPubMed
34.
go back to reference Rusconi F, Galassi C, Forastiere F, Bellasio M, De Sario M, Ciccone G, Brunetti L, Chellini E, Corbo G, La Grutta S, Lombardi E, Piffer S, Talassi F, Biggeri A, Pearce N: Maternal complications and procedures in pregnancy and at birth and wheezing phenotypes in children. Am J Respir Crit Care Med. 2007, 175 (1): 16-21. 10.1164/rccm.200512-1978OC.CrossRefPubMed Rusconi F, Galassi C, Forastiere F, Bellasio M, De Sario M, Ciccone G, Brunetti L, Chellini E, Corbo G, La Grutta S, Lombardi E, Piffer S, Talassi F, Biggeri A, Pearce N: Maternal complications and procedures in pregnancy and at birth and wheezing phenotypes in children. Am J Respir Crit Care Med. 2007, 175 (1): 16-21. 10.1164/rccm.200512-1978OC.CrossRefPubMed
35.
go back to reference Lum S, Hoo AF, Dezateux C, Goetz I, Wade A, DeRooy L, Costeloe K, Stocks J: The association between birthweight, sex, and airway function in infants of nonsmoking mothers. Am J Respir Crit Care Med. 2001, 164 (11): 2078-2084. 10.1164/ajrccm.164.11.2104053.CrossRefPubMed Lum S, Hoo AF, Dezateux C, Goetz I, Wade A, DeRooy L, Costeloe K, Stocks J: The association between birthweight, sex, and airway function in infants of nonsmoking mothers. Am J Respir Crit Care Med. 2001, 164 (11): 2078-2084. 10.1164/ajrccm.164.11.2104053.CrossRefPubMed
36.
go back to reference Rondon C, Campo P, Galindo L, Blanca-Lopez N, Cassinello MS, Rodriguez-Bada JL, Torres MJ, Blanca M: Prevalence and clinical relevance of local allergic rhinitis. Allergy. 2012, 67 (10): 1282-1288. 10.1111/all.12002.CrossRefPubMed Rondon C, Campo P, Galindo L, Blanca-Lopez N, Cassinello MS, Rodriguez-Bada JL, Torres MJ, Blanca M: Prevalence and clinical relevance of local allergic rhinitis. Allergy. 2012, 67 (10): 1282-1288. 10.1111/all.12002.CrossRefPubMed
37.
go back to reference Robins JM, Greenland S: Identifiability and exchangeability for direct and indirect effects. Epidemiology. 1992, 3 (2): 143-155. 10.1097/00001648-199203000-00013.CrossRefPubMed Robins JM, Greenland S: Identifiability and exchangeability for direct and indirect effects. Epidemiology. 1992, 3 (2): 143-155. 10.1097/00001648-199203000-00013.CrossRefPubMed
Metadata
Title
Birth after preeclamptic pregnancies: association with allergic sensitization and allergic rhinoconjunctivitis in late childhood; a historically matched cohort study
Authors
Kristine Kjer Byberg
Bjorn Ogland
Geir Egil Eide
Knut Øymar
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Pediatrics / Issue 1/2014
Electronic ISSN: 1471-2431
DOI
https://doi.org/10.1186/1471-2431-14-101

Other articles of this Issue 1/2014

BMC Pediatrics 1/2014 Go to the issue