Modifiable prenatal environmental factors for the prevention of childhood asthma

Hyo-Bin Kim

doi:10.4168/aard.2019.7.4.179

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Kim: Modifiable prenatal environmental factors for the prevention of childhood asthma

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Allergy, Asthma & Respiratory Disease 2019; 7(4): 179-185.

Published online: 30 October 2019

DOI: https://doi.org/10.4168/aard.2019.7.4.179

Modifiable prenatal environmental factors for the prevention of childhood asthma

Hyo-Bin Kim

Department of Pediatrics, Inje University Sanggye Paik Hospital, Seoul, Korea.

Correspondence to: Hyo-Bin Kim. Department of Pediatrics, Inje University Sanggye Paik Hospital, 1342 Dongil-ro, Nowon-gu, Seoul 01757, Korea. Tel: +82-2-950-1663, Fax: +82-2-950-1662, hbkim@paik.ac.kr

Received 17 March 2019 Revised 11 May 2019 Accepted 14 May 2019

The Korean Academy of Pediatric Allergy and Respiratory Disease; The Korean Academy of Asthma, Allergy and Clinical Immunology

(open-access):

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/).

Abstract

The prevalence of asthma in children is increasing worldwide, yet risk factors for the development of asthma is unclear. Evidence to date indicates that environmental factors are the main reason of the recent increase in the prevalence of asthma. For example, exposure to air pollution and diet as well as microbial alterations are reported as environmental factors. In addition, we should focus on the critical period of the exposure, especially pregnancy period as an important period for human development. Therefore, environmental exposure during pregnancy to tobacco smoke or air pollutants, maternal stress, obesity, and vitamin D may contribute to the development of childhood asthma. Herein, modifiable prenatal exposure, its mechanisms associated with childhood asthma and multiple intervention controlling risk factors needed during pregnancy in order to achieve primary prevention of asthma has been described.

Keywords: Asthma, Child, Environment, Pregnancy, Risk factor

Figures and Tables

Fig. 1

Environmental factors exposed during pregnancy that may influence on the development of childhood asthma.

References

1. Eder W, Ege MJ, von Mutius E. The asthma epidemic. N Engl J Med. 2006; 355:2226–2235.

2. Martino D, Prescott S. Epigenetics and prenatal influences on asthma and allergic airways disease. Chest. 2011; 139:640–647.

3. Yang HJ. Impact of perinatal environmental tobacco smoke on the development of childhood allergic diseases. Korean J Pediatr. 2016; 59:319–327.

4. Moorman JE, Akinbami LJ, Bailey CM, Zahran HS, King ME, Johnson CA, et al. National surveillance of asthma: United States, 2001–2010. Vital Health Stat 3. 2012; (35):1–58.

5. Hong SJ, Ahn KM, Lee SY, Kim KE. The prevalences of asthma and allergic diseases in Korean children. Korean J Pediatr. 2008; 51:343–350.

6. Lee Y, Choi J, Park MR, Kim J, Kim WK, Park YM, et al. Analysis of regional prevalence of allergic diseases in Korean school children. Allergy Asthma Respir Dis. 2015; 3:62–69.

7. Cecchi L, D'Amato G, Annesi-Maesano I. External exposome and allergic respiratory and skin diseases. J Allergy Clin Immunol. 2018; 141:846–857.

8. Rosas-Salazar C, Hartert TV. Prenatal exposures and the development of childhood wheezing illness. Curr Opin Allergy Clin Immunol. 2017; 17:110–115.

9. Abreo A, Gebretsadik T, Stone CA, Hartert TV. The impact of modifiable risk factor reduction on childhood asthma development. Clin Transl Med. 2018; 7:15.

10. Yang HJ, Lee SY, Suh DI, Shin YH, Kim BJ, Seo JH, et al. The Cohort for Childhood Origin of Asthma and allergic diseases (COCOA) study: design, rationale and methods. BMC Pulm Med. 2014; 14:109.

11. Maitre L, de Bont J, Casas M, Robinson O, Aasvang GM, Agier L, et al. Human Early Life Exposome (HELIX) study: a European population-based exposome cohort. BMJ Open. 2018; 8:e021311.

12. Grieger JA, Clifton VL, Tuck AR, Wooldridge AL, Robertson SA, Gatford KL. In utero programming of allergic susceptibility. Int Arch Allergy Immunol. 2016; 169:80–92.

13. Burke H, Leonardi-Bee J, Hashim A, Pine-Abata H, Chen Y, Cook DG, et al. Prenatal and passive smoke exposure and incidence of asthma and wheeze: systematic review and meta-analysis. Pediatrics. 2012; 129:735–744.

14. Vardavas CI, Hohmann C, Patelarou E, Martinez D, Henderson AJ, Granell R, et al. The independent role of prenatal and postnatal exposure to active and passive smoking on the development of early wheeze in children. Eur Respir J. 2016; 48:115–124.

15. Henderson AJ, Sherriff A, Northstone K, Kukla L, Hruba D. Pre- and postnatal parental smoking and wheeze in infancy: cross cultural differences. Avon Study of Parents and Children (ALSPAC) Study Tem, European Longitudinal Study of Pregnancy and Childhood (ELSPAC) Co-ordinating Centre. Eur Respir J. 2001; 18:323–329.

16. Harju M, Keski-Nisula L, Georgiadis L, Heinonen S. Parental smoking and cessation during pregnancy and the risk of childhood asthma. BMC Public Health. 2016; 16:428.

17. Hehua Z, Qing C, Shanyan G, Qijun W, Yuhong Z. The impact of prenatal exposure to air pollution on childhood wheezing and asthma: a systematic review. Environ Res. 2017; 159:519–530.

18. Morales E, Garcia-Esteban R, de la, Basterrechea M, Lertxundi A, de Dicastillo MD, et al. Intrauterine and early postnatal exposure to outdoor air pollution and lung function at preschool age. Thorax. 2015; 70:64–73.

19. Nobles CJ, Grantz KL, Liu D, Williams A, Ouidir M, Seeni I, et al. Ambient air pollution and fetal growth restriction: physician diagnosis of fetal growth restriction versus population-based small-for-gestational age. Sci Total Environ. 2019; 650:2641–2647.

20. Lavigne E, Belair MA, Rodriguez Duque D, Do MT, Stieb DM, Hystad P, et al. Effect modification of perinatal exposure to air pollution and childhood asthma incidence. Eur Respir J. 2018; 02. 01. [Epub ahead of print].

21. Hsu HH, Chiu YH, Coull BA, Kloog I, Schwartz J, Lee A, et al. Prenatal particulate air pollution and asthma onset in urban children. Identifying sensitive windows and sex differences. Am J Respir Crit Care Med. 2015; 192:1052–1059.

22. Lee A, Hsu HH, Chiu YH, Bose S, Rosa MJ, Kloog I, et al. Prenatal fine particulate exposure and early childhood asthma: effect of maternal stress and fetal sex. J Allergy Clin Immunol. 2018; 141:1880–1886.

23. Gruzieva O, Xu CJ, Breton CV, Annesi-Maesano I, Anto JM, Auffray C, et al. Epigenome-wide meta-analysis of methylation in children related to prenatal NO2 air pollution exposure. Environ Health Perspect. 2017; 125:104–110.

24. Makamure MT, Reddy P, Chuturgoon A, Naidoo RN, Mentz G, Batterman S, et al. Tumour necrosis factor α polymorphism (TNF-308α G/A) in association with asthma related phenotypes and air pollutants among children in KwaZulu-Natal. Asian Pac J Allergy Immunol. 2016; 34:217–222.

25. Alexis NE, Zhou H, Lay JC, Harris B, Hernandez ML, Lu TS, et al. The glutathione-S-transferase Mu 1 null genotype modulates ozone-induced airway inflammation in human subjects. J Allergy Clin Immunol. 2009; 124:1222–1228.

26. Rosa MJ, Just AC, Tamayo Y, Schnaas L, Svensson K, Wright RO, et al. Prenatal and postnatal stress and wheeze in Mexican children: sex-specific differences. Ann Allergy Asthma Immunol. 2016; 116:306–312.

27. Andersson NW, Hansen MV, Larsen AD, Hougaard KS, Kolstad HA, Schlunssen V. Prenatal maternal stress and atopic diseases in the child: a systematic review of observational human studies. Allergy. 2016; 71:15–26.

28. van de Loo KF, van Gelder MM, Roukema J, Roeleveld N, Merkus PJ, Verhaak CM. Prenatal maternal psychological stress and childhood asthma and wheezing: a meta-analysis. Eur Respir J. 2016; 47:133–146.

29. Flanigan C, Sheikh A, DunnGalvin A, Brew BK, Almqvist C, Nwaru BI. Prenatal maternal psychosocial stress and offspring's asthma and allergic disease: a systematic review and meta-analysis. Clin Exp Allergy. 2018; 48:403–414.

30. von Hertzen LC. Maternal stress and T-cell differentiation of the developing immune system: possible implications for the development of asthma and atopy. J Allergy Clin Immunol. 2002; 109:923–928.

31. Trump S, Bieg M, Gu Z, Thurmann L, Bauer T, Bauer M, et al. Prenatal maternal stress and wheeze in children: novel insights into epigenetic regulation. Sci Rep. 2016; 6:28616.

32. Azad MB, Kozyrskyi AL. Perinatal programming of asthma: the role of gut microbiota. Clin Dev Immunol. 2012; 2012:932072.

33. Han YY, Forno E, Holguin F, Celedon JC. Diet and asthma: an update. Curr Opin Allergy Clin Immunol. 2015; 15:369–374.

34. von Ehrenstein OS, Aralis H, Flores ME, Ritz B. Fast food consumption in pregnancy and subsequent asthma symptoms in young children. Pediatr Allergy Immunol. 2015; 26:571–577.

35. Beckhaus AA, Garcia-Marcos L, Forno E, Pacheco-Gonzalez RM, Celedon JC, Castro-Rodriguez JA. Maternal nutrition during pregnancy and risk of asthma, wheeze, and atopic diseases during childhood: a systematic review and meta-analysis. Allergy. 2015; 70:1588–1604.

36. Looker AC, Johnson CL, Lacher DA, Pfeiffer CM, Schleicher RL, Sempos CT. Vitamin D status: United States, 2001-2006. NCHS Data Brief. 2011; (59):1–8.

37. Wegienka G, Havstad S, Zoratti EM, Kim H, Ownby DR, Johnson CC. Association between vitamin D levels and allergy-related outcomes vary by race and other factors. J Allergy Clin Immunol. 2015; 136:1309–1314.

38. Visness CM, Sandel MT, O'Connor G, Gern JE, Jaffee KF, Wood RA, et al. Cord blood vitamin D concentrations are unrelated to atopy and wheeze in 2 diverse birth cohort studies. J Allergy Clin Immunol. 2015; 136:1108–1110.

39. Chawes BL, Bonnelykke K, Stokholm J, Vissing NH, Bjarnadottir E, Schoos AM, et al. Effect of vitamin D3 supplementation during pregnancy on risk of persistent wheeze in the offspring: a randomized clinical trial. JAMA. 2016; 315:353–361.

40. Litonjua AA, Carey VJ, Laranjo N, Harshfield BJ, McElrath TF, O'Connor GT, et al. Effect of prenatal supplementation with vitamin D on asthma or recurrent wheezing in offspring by age 3 years: the VDAART randomized clinical trial. JAMA. 2016; 315:362–370.

41. Wolsk HM, Chawes BL, Litonjua AA, Hollis BW, Waage J, Stockholm J, et al. Prenatal vitamin D supplementation reduces risk of asthma/recurrent wheeze in early childhood: a combined analysis of two randomized controlled trials. PLoS ONE. 2017; 12:e0186657.

42. Devereux G, Craig L, Seaton A, Turner S. Maternal vitamin D and E intakes in pregnancy and asthma to age 15 years: a cohort study. Pediatr Pulmonol. 2019; 54:11–19.

43. Zosky GR, Berry LJ, Elliot JG, James AL, Gorman S, Hart PH. Vitamin D deficiency causes deficits in lung function and alters lung structure. Am J Respir Crit Care Med. 2011; 183:1336–1343.

44. Mirzakhani H, Al-Garawi A, Weiss ST, Litonjua AA. Vitamin D and the development of allergic disease: how important is it? Clin Exp Allergy. 2015; 45:114–125.

45. Bosse Y, Lemire M, Poon AH, Daley D, He JQ, Sandford A, et al. Asthma and genes encoding components of the vitamin D pathway. Respir Res. 2009; 10:98.

46. Ferreira GB, Vanherwegen AS, Eelen G, Gutierrez ACF, Van Lommel L, Marchal K, et al. Vitamin D3 induces tolerance in human dendritic cells by activation of intracellular metabolic pathways. Cell Rep. 2015; 10:711–725.

47. Wu H, Zhang C, Wang Y, Li Y. Does vitamin E prevent asthma or wheeze in children: a systematic review and meta-analysis. Paediatr Respir Rev. 2018; 27:60–68.

48. Bailey RL, Fulgoni VL 3rd, Keast DR, Dwyer JT. Examination of vitamin intakes among US adults by dietary supplement use. J Acad Nutr Diet. 2012; 112:657–663.

49. Veeranki SP, Gebretsadik T, Mitchel EF, Tylavsky FA, Hartert TV, Cooper WO, et al. Maternal folic acid supplementation during pregnancy and early childhood asthma. Epidemiology. 2015; 26:934–941.

50. Wang T, Zhang HP, Zhang X, Liang ZA, Ji YL, Wang G. Is folate status a risk factor for asthma or other allergic diseases? Allergy Asthma Immunol Res. 2015; 7:538–546.

51. Roy A, Kocak M, Hartman TJ, Vereen S, Adgent M, Piyathilake C, et al. Association of prenatal folate status with early childhood wheeze and atopic dermatitis. Pediatr Allergy Immunol. 2018; 29:144–150.

52. Alfonso VH, Bandoli G, von Ehrenstein O, Ritz B. Early folic acid supplement initiation and risk of adverse early childhood respiratory health: a population-based study. Matern Child Health J. 2018; 22:111–119.

53. Joshi R, Adhikari S, Patro BS, Chattopadhyay S, Mukherjee T. Free radical scavenging behavior of folic acid: evidence for possible antioxidant activity. Free Radic Biol Med. 2001; 30:1390–1399.

54. Dhur A, Galan P, Hercberg S. Folate status and the immune system. Prog Food Nutr Sci. 1991; 15:43–60.

55. Gunaratne AW, Makrides M, Collins CT. Maternal prenatal and/or postnatal n-3 long chain polyunsaturated fatty acids (LCPUFA) supplementation for preventing allergies in early childhood. Cochrane Database Syst Rev. 2015; CD010085.

56. Rucci E, den Dekker HT, de Jongste JC, Steenweg-de-Graaff J, Gaillard R, Pasmans SG, et al. Maternal fatty acid levels during pregnancy, childhood lung function and atopic diseases. The generation R study. Clin Exp Allergy. 2016; 46:461–471.

57. Ledger WJ, Blaser MJ. Are we using too many antibiotics during pregnancy? BJOG. 2013; 120:1450–1452.

58. Zhao D, Su H, Cheng J, Wnag X, Xie M, Li K, et al. Prenatal antibiotic use and risk of childhood wheeze/asthma: a meta-analysis. Pediatr Allergy Immunol. 2015; 26:756–764.

59. Wu P, Feldman AS, Rosas-Salazar C, James K, Escobar G, Gebretsadik T, et al. Relative importance and additive effects of maternal and infant risk factors on childhood asthma. PLoS ONE. 2016; 11:e0151705.

60. Fleming-Dutra KE, Hersh AL, Shapiro DJ, Bartoces M, Enns EA, File TM Jr, et al. Prevalence of inappropriate antibiotic prescriptions among US ambulatory care visits, 2010-2011. JAMA. 2016; 315:1864–1873.

61. Lynch SV, Pedersen O. The human intestinal microbiome in health and disease. N Engl J Med. 2016; 375:2369–2379.

62. Huang YJ, Boushey HA. The microbiome in asthma. J Allergy Clin Immunol. 2015; 135:25–30.

63. Fricke WF. The more the merrier? Reduced fecal microbiota diversity in preterm infants treated with antibiotics. J Pediatr. 2014; 165:8–10.

64. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA. 2010; 107:11971–11975.

65. Keag OE, Norman JE, Stock SJ. Long-term risks and benefits associated with cesarean delivery for mother, baby, and subsequent pregnancies: systematic review and meta-analysis. PLoS Med. 2018; 15:e1002494.

66. Lee E, Kim JB, Kang MJ, Choi KY, Cho JH, Kim Y, et al. Dynamics of gut microbiota according to the delivery mode in healthy Korean infants. Allergy Asthma Immunol Res. 2016; 8:471–477.

67. Murgas Torrazza R, Neu J. The developing intestinal microbiome and its relationship to health and disease in the neonate. J Perinatol. 2011; 31 Suppl 1:S29–S34.

68. Ball TM, Castro-Rodriguez JA, Griffith KA, Holberg CJ, Martinez FD, Wright AL. Siblings, day-care attendance, and the risk of asthma and wheezing during childhood. N Engl J Med. 2000; 343:538–543.

69. Midodzi WK, Rowe BH, Majaesic CM, Saunders LD, Senthilselvan A. Early life factors associated with incidence of physician-diagnosed asthma in preschool children: results from the Canadian Early Childhood Development cohort study. J Asthma. 2010; 47:7–13.

70. Ege MJ, Mayer M, Normand AC, Genuneit J, Cookson WO, Braun-Fahrlander C, et al. Exposure to environmental microorganisms and childhood asthma. N Engl J Med. 2011; 364:701–709.

71. Zugna D, Galassi C, Annesi-Maesano I, Baiz N, Barros H, Basterrechea M, et al. Maternal complications in pregnancy and wheezing in early childhood: a pooled analysis of 14 birth cohorts. Int J Epidemiol. 2015; 44:199–208.

72. Rusconi F, Popovic M. Maternal obesity and childhood wheezing and asthma. Paediatr Respir Rev. 2017; 22:66–71.

73. Haberg SE, Stigum H, London SJ, Nystad W, Nafstad P. Maternal obesity in pregnancy and respiratory health in early childhood. Paediatr Perinat Epidemiol. 2009; 23:352–362.

74. Eising JB, Uiterwaal CS, van der. Maternal body mass index, neonatal lung function and respiratory symptoms in childhood. Eur Respir J. 2015; 46:1342–1349.

75. Pike KC, Inskip HM, Robinson SM, Cooper C, Godfrey KM, Roberts G, et al. the relationship between maternal adiposity and infant weight gain, and childhood wheeze and atopy. Thorax. 2013; 68:372–379.

76. Harpsoe MC, Basit S, Bager P, Wohlfahrt J, Benn CS, Nohr EA, et al. Maternal obesity, gestational weight gain, and risk of asthma and atopic disease in offspring: a study within the Danish National Birth Cohort. J Allergy Clin Immunol. 2013; 131:1033–1040.

77. Dumas O, Varraso R, Gillman MW, Field AE, Camargo CA Jr. Longitudinal study of maternal body mass index, gestational weight gain, and offspring asthma. Allergy. 2016; 71:1295–1304.

78. Halonen M, Lohman IC, Stern DA, Ellis WL, Rothers J, Wright AL. Perinatal tumor necrosis factor-α production, influenced by maternal pregnancy weight gain, predicts childhood asthma. Am J Respir Crit Care Med. 2013; 188:35–41.

79. Morales E, Guerra S, Garcia-Esteban R, Guxens M, Alvarez-Pedrerol M, Bustamante M, et al. Maternal C-reactive protein levels in pregnancy are associated with wheezing and lower respiratory tract infections in the offspring. Am J Obstet Gynecol. 2011; 204:164.

80. Hendler I, Blackwell SC, Mehta SH, Whitty JE, Russell E, Sorokin Y, et al. The levels of leptin, adiponectin, and resistin in normal weight, overweight, and obese pregnant women with and without preeclampsia. Am J Obstet Gynecol. 2005; 193(3 Pt 2):979–983.

81. Chatzi L, Garcia R, Roumeliotaki T, Basterrechea M, Begiristain H, Iniguez C, et al. Mediterranean diet adherence during pregnancy and risk of wheeze and eczema in the first year of life: INMA (Spain) and RHEA (Greece) mother-child cohort studies. Br J Nutr. 2013; 110:2058–2068.

82. Miyake Y, Sasaki S, Tanaka K, Ohfuji S, Hirota Y. Maternal fat consumption during pregnancy and risk of wheeze and eczema in Japanese infants aged 16-24 months: the Osaka Maternal and Child Health Study. Thorax. 2009; 64:815–821.

83. Scholl TO, Chen X. Vitamin D intake during pregnancy: association with maternal characteristics and infant birth weight. Early Hum Dev. 2009; 85:231–234.

84. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006; 444:1022–1023.

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ORCID iDs: Hyo-Bin Kim
https://orcid.org/0000-0002-1928-722X
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