Preterm birth and childhood wheezing disorders: a systematic review and meta-analysis

Jasper V Been, Marlies J Lugtenberg, Eline Smets, Constant P van Schayck, Boris W Kramer, Monique Mommers, Aziz Sheikh, Jasper V Been, Marlies J Lugtenberg, Eline Smets, Constant P van Schayck, Boris W Kramer, Monique Mommers, Aziz Sheikh

Abstract

Background: Accumulating evidence implicates early life factors in the aetiology of non-communicable diseases, including asthma/wheezing disorders. We undertook a systematic review investigating risks of asthma/wheezing disorders in children born preterm, including the increasing numbers who, as a result of advances in neonatal care, now survive very preterm birth.

Methods and findings: Two reviewers independently searched seven online databases for contemporaneous (1 January 1995-23 September 2013) epidemiological studies investigating the association between preterm birth and asthma/wheezing disorders. Additional studies were identified through reference and citation searches, and contacting international experts. Quality appraisal was undertaken using the Effective Public Health Practice Project instrument. We pooled unadjusted and adjusted effect estimates using random-effects meta-analysis, investigated "dose-response" associations, and undertook subgroup, sensitivity, and meta-regression analyses to assess the robustness of associations. We identified 42 eligible studies from six continents. Twelve were excluded for population overlap, leaving 30 unique studies involving 1,543,639 children. Preterm birth was associated with an increased risk of wheezing disorders in unadjusted (13.7% versus 8.3%; odds ratio [OR] 1.71, 95% CI 1.57-1.87; 26 studies including 1,500,916 children) and adjusted analyses (OR 1.46, 95% CI 1.29-1.65; 17 studies including 874,710 children). The risk was particularly high among children born very preterm (<32 wk gestation; unadjusted: OR 3.00, 95% CI 2.61-3.44; adjusted: OR 2.81, 95% CI 2.55-3.12). Findings were most pronounced for studies with low risk of bias and were consistent across sensitivity analyses. The estimated population-attributable risk of preterm birth for childhood wheezing disorders was ≥3.1%. Key limitations related to the paucity of data from low- and middle-income countries, and risk of residual confounding.

Conclusions: There is compelling evidence that preterm birth-particularly very preterm birth-increases the risk of asthma. Given the projected global increases in children surviving preterm births, research now needs to focus on understanding underlying mechanisms, and then to translate these insights into the development of preventive interventions.

Review registration: PROSPERO CRD42013004965.

Conflict of interest statement

AS is a member of the Editorial Board of PLOS Medicine. The authors have declared that no other competing interests exist.

Figures

Figure 1. Flowchart outlining study selection.
Figure 1. Flowchart outlining study selection.
WHO GHL, World Health Organization Global Health Library; WHOLIS, World Health Organization Library Information System.
Figure 2. Meta-analysis of unadjusted association between…
Figure 2. Meta-analysis of unadjusted association between preterm birth and childhood wheezing disorders.
Heterogeneity: I2 = 82% (95% CI 75%–87%). PTB, preterm birth; WD, wheezing disorders.
Figure 3. Meta-analysis of adjusted association between…
Figure 3. Meta-analysis of adjusted association between preterm birth and childhood wheezing disorders.
Subgroups taken from individual studies noted in parentheses. Heterogeneity: I2 = 80% (95% CI 68%–86%). Individual study adjustment for the primary confounders is depicted. Additional confounders adjusted for are outlined in Table S3. FH, family history; LRI, lower respiratory infection; PTB, preterm birth; WD, wheezing disorders.
Figure 4. Meta-analysis of adjusted dose–response association…
Figure 4. Meta-analysis of adjusted dose–response association between gestational age (per week increase) and childhood wheezing disorders.
Heterogeneity: I2 = 90% (95% CI 85%–92%). Individual study adjustment for the primary confounders is depicted. Additional confounders adjusted for are outlined in Table S3. FH, family history; WD, wheezing disorders.
Figure 5. Meta-analysis of association between very…
Figure 5. Meta-analysis of association between very preterm birth and childhood wheezing disorders.
(A) unadjusted effect estimates; (B) adjusted effect estimates. Subgroups taken from individual studies noted in parentheses. Heterogeneity: I2 (unadjusted) = 62% (95% CI 9%–79%); I2 (adjusted) = 0% (95% CI 0%–68%). Confounders adjusted for in individual studies are outlined in Figure 3 and Table S3. LRI, lower respiratory infection; PTB, preterm birth; WD, wheezing disorders.
Figure 6. Meta-analysis of association between moderately…
Figure 6. Meta-analysis of association between moderately preterm birth and childhood wheezing disorders.
(A) unadjusted effect estimates; (B) adjusted effect estimates. Subgroups taken from individual studies noted in parentheses. Heterogeneity: I2 (unadjusted) = 92% (95% CI 87%–94%); I2 (adjusted) = 89% (95% CI 82%–93%). Confounders adjusted for in individual studies are outlined in Figure 3 and Table S3. LRI, lower respiratory infection; PTB, preterm birth; WD, wheezing disorders.
Figure 7. Funnel plots for studies reporting…
Figure 7. Funnel plots for studies reporting unadjusted and adjusted association measures.
(A) unadjusted association measures; (B) adjusted association measures.

References

    1. Gluckman PD, Hanson MA, Cooper C, Thornburg KL (2008) Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 359: 61–73.
    1. Blencowe H, Cousens S, Oestergaard MZ, Chou D, Moller AB, et al. (2012) National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications. Lancet 379: 2162–2172.
    1. Chang HH, Larson J, Blencowe H, Spong CY, Howson CP, et al. (2013) Preventing preterm births: analysis of trends and potential reductions with interventions in 39 countries with very high human development index. Lancet 381: 223–234.
    1. Jobe AH (2010) “Miracle” extremely low birth weight neonates: examples of developmental plasticity. Obstet Gynecol 116: 1184–1190.
    1. Jobe AH (2011) The new bronchopulmonary dysplasia. Curr Opin Pediatr 23: 167–172.
    1. Colin AA, McEvoy C, Castile RG (2010) Respiratory morbidity and lung function in preterm infants of 32 to 36 weeks' gestational age. Pediatrics 126: 115–128.
    1. Kotecha SJ, Edwards MO, Watkins WJ, Henderson AJ, Paranjothy S, et al. (2013) Effect of preterm birth on later FEV1: a systematic review and meta-analysis. Thorax 68: 760–766.
    1. Brostrom EB, Akre O, Katz-Salamon M, Jaraj D, Kaijser M (2013) Obstructive pulmonary disease in old age among individuals born preterm. Eur J Epidemiol 28: 79–85.
    1. Jaakkola JJ, Ahmed P, Ieromnimon A, Goepfert P, Laiou E, et al. (2006) Preterm delivery and asthma: a systematic review and meta-analysis. J Allergy Clin Immunol 118: 823–830.
    1. Anandan C, Nurmatov U, van Schayck OC, Sheikh A (2010) Is the prevalence of asthma declining? Systematic review of epidemiological studies. Allergy 65: 152–167.
    1. Robison RG, Singh AM (2013) Chapter 11: the infant and toddler with wheezing. Allergy Asthma Proc 33: S36–S38.
    1. (2013) Trip [database]. Available: . Accessed 22 September 2013.
    1. Nurmatov U, Devereux G, Sheikh A (2011) Nutrients and foods for the primary prevention of asthma and allergy: systematic review and meta-analysis. J Allergy Clin Immunol 127: 724–733.
    1. Effective Public Health Practice Project (2013) Quality assessment tool for quantitative studies. Available: . Accessed 2 May 2013.
    1. Higgins JP, Green S (2011) Cochrane handbook for systematic reviews of interventions. Oxford: The Cochrane Collaboration.
    1. Berlin JA, Longnecker MP, Greenland S (1993) Meta-analysis of epidemiologic dose-response data. Epidemiology 4: 218–228.
    1. Rockhill B, Newman B, Weinberg C (1998) Use and misuse of population attributable fractions. Am J Public Health 88: 15–19.
    1. Alm B, Erdes L, Mollborg P, Pettersson R, Norvenius SG, et al. (2008) Neonatal antibiotic treatment is a risk factor for early wheezing. Pediatrics 121: 697–702.
    1. Alvarez Mingorance P, Buron Martinez E, Blanco Quiros A (2011) Morbilidad de los niños prematuros en edad escolar (II): patología respiratoria, alteraciones del crecimiento y presión arterial. Acta Pediatr Esp 69: 235–240.
    1. Aspberg S, Dahlquist G, Kahan T, Kallen B (2010) Confirmed association between neonatal phototherapy or neonatal icterus and risk of childhood asthma. Pediatr Allergy Immunol 21: e733–e739.
    1. Bérard A, Le Tiec M, De Vera MA (2012) Study of the costs and morbidities of late-preterm birth. Arch Dis Child Fetal Neonatal Ed 97: F329–F334.
    1. Boyle EM, Poulsen G, Field DJ, Kurinczuk JJ, Wolke D, et al. (2012) Effects of gestational age at birth on health outcomes at 3 and 5 years of age: population based cohort study. BMJ 344: e896.
    1. Brehm JM, Acosta-Perez E, Klei L, Roeder K, Barmada M, et al. (2012) Vitamin D insufficiency and severe asthma exacerbations in Puerto Rican children. Am J Respir Crit Care Med 186: 140–146.
    1. Castro-Rodriguez JA, Garcia-Marcos L, Sanchez-Solis M, Perez-Fernandez V, Martinez-Torres A, et al. (2010) Olive oil during pregnancy is associated with reduced wheezing during the first year of life of the offspring. Pediatr Pulmonol 45: 395–402.
    1. Cheraghi M, Dadgarinejad A, Salvi S (2012) A cross-sectional study to find prevalence and risk factors for childhood asthma in Pune City, India. ISRN Public Health 2012: 361456.
    1. Civelek E, Cakir B, Orhan F, Yuksel H, Boz AB, et al. (2011) Risk factors for current wheezing and its phenotypes among elementary school children. Pediatr Pulmonol 46: 166–174.
    1. Collier CH, Risnes K, Norwitz ER, Bracken MB, Illuzzi JL (2013) Maternal infection in pregnancy and risk of asthma in offspring. Matern Child Health J 17: 1940–1950 doi:
    1. Escobar GJ, Ragins A, Li SX, Prager L, Masaquel AS, et al. (2010) Recurrent wheezing in the third year of life among children born at 32 weeks' gestation or later: relationship to laboratory-confirmed, medically attended infection with respiratory syncytial virus during the first year of life. Arch Pediatr Adolesc Med 164: 915–922.
    1. Fawke J, Lum S, Kirkby J, Hennessy E, Marlow N, et al. (2010) Lung function and respiratory symptoms at 11 years in children born extremely preterm: the EPICure study. Am J Respir Crit Care Med 182: 237–245.
    1. Gessner BD, Chimonas MA (2007) Asthma is associated with preterm birth but not with small for gestational age status among a population-based cohort of Medicaid-enrolled children <10 years of age. Thorax 62: 231–236.
    1. Getahun D, Strickland D, Zeiger RS, Fassett MJ, Chen W, et al. (2010) Effect of chorioamnionitis on early childhood asthma. Arch Pediatr Adolesc Med 164: 187–192.
    1. Gorman BK, Landale NS (2005) Premature birth and asthma among young Puerto Rican children. Popul Res Policy Rev 24: 335–358.
    1. Goyal NK, Fiks AG, Lorch SA (2011) Association of late-preterm birth with asthma in young children: practice-based study. Pediatrics 128: e830–e838.
    1. Hennessy EM, Bracewell MA, Wood N, Wolke D, Costeloe K, et al. (2008) Respiratory health in pre-school and school age children following extremely preterm birth. Arch Dis Child 93: 1037–1043.
    1. Joshi S, Powell T, Watkins WJ, Drayton M, Williams EM, et al. (2013) Exercise-induced bronchoconstriction in school-aged children who had chronic lung disease in infancy. J Pediatr 162: 813–818.
    1. Källén B, Finnstrom O, Nygren KG, Otterblad Olausson P (2013) Association between preterm birth and intrauterine growth retardation and child asthma. Eur Respir J 41: 671–676.
    1. Kang EM, Lundsberg LS, Illuzzi JL, Bracken MB (2009) Prenatal exposure to acetaminophen and asthma in children. Obstet Gynecol 114: 1295–1306.
    1. Koshy G, Akrouf KA, Kelly Y, Delpisheh A, Brabin BJ (2013) Asthma in children in relation to pre-term birth and fetal growth restriction. Matern Child Health J 17: 1119–1126.
    1. Kumar R, Yu Y, Story RE, Pongracic JA, Gupta R, et al. (2008) Prematurity, chorioamnionitis, and the development of recurrent wheezing: a prospective birth cohort study. J Allergy Clin Immunol 121: 878–884.
    1. Kumar R, Tsai HJ, Hong X, Gignoux C, Pearson C, et al. (2012) African ancestry, early life exposures, and respiratory morbidity in early childhood. Clin Exp Allergy 42: 265–274.
    1. Lum S, Kirkby J, Welsh L, Marlow N, Hennessy E, et al. (2011) Nature and severity of lung function abnormalities in extremely pre-term children at 11 years of age. Eur Respir J 37: 1199–1207.
    1. Miyake Y, Tanaka K (2013) Lack of relationship between birth conditions and allergic disorders in Japanese children aged 3 years. J Asthma 50: 555–559.
    1. Rautava L, Hakkinen U, Korvenranta E, Andersson S, Gissler M, et al. (2010) Health and the use of health care services in 5-year-old very-low-birth-weight infants. Acta Paediatr 99: 1073–1079.
    1. Robison RG, Kumar R, Arguelles LM, Hong X, Wang G, et al. (2012) Maternal smoking during pregnancy, prematurity and recurrent wheezing in early childhood. Pediatr Pulmonol 47: 666–673.
    1. Taveras EM, Camargo CA Jr, Rifas-Shiman SL, Oken E, Gold DR, et al. (2006) Association of birth weight with asthma-related outcomes at age 2 years. Pediatr Pulmonol 41: 643–648.
    1. Visser CA, Garcia-Marcos L, Eggink J, Brand PL (2010) Prevalence and risk factors of wheeze in Dutch infants in their first year of life. Pediatr Pulmonol 45: 149–156.
    1. Vogt H, Lindstrom K, Braback L, Hjern A (2011) Preterm birth and inhaled corticosteroid use in 6- to 19-year-olds: a Swedish national cohort study. Pediatrics 127: 1052–1059.
    1. Vrijlandt EJ, Kerstjens JM, Duiverman EJ, Bos AF, Reijneveld SA (2013) Moderate preterm children have more respiratory problems during their first five years of life than children born full term. Am J Respir Crit Care Med 187: 1234–1240.
    1. Welsh L, Kirkby J, Lum S, Odendaal D, Marlow N, et al. (2009) The EPICure study: maximal exercise and physical activity in school children born extremely preterm. Thorax 65: 165–172.
    1. Yang KD, Ou CY, Chang JC, Chen RF, Liu CA, et al. (2007) Infant frequent wheezing correlated to Clara cell protein 10 (CC10) polymorphism and concentration, but not allergy sensitization, in a perinatal cohort study. J Allergy Clin Immunol 120: 842–848.
    1. Yuan W, Fonager K, Olsen J, Sorensen HT (2003) Prenatal factors and use of anti-asthma medications in early childhood: a population-based Danish birth cohort study. Eur J Epidemiol 18: 763–768.
    1. Algert CS, Bowen JR, Lain SL, Allen HD, Vivian-Taylor JM, et al. (2011) Pregnancy exposures and risk of childhood asthma admission in a population birth cohort. Pediatr Allergy Immunol 22: 836–842.
    1. Koshy G, Delpisheh A, Brabin BJ (2010) Trends in prevalence of childhood and parental asthma in Merseyside, 1991–2006. J Public Health (Oxf) 32: 488–495.
    1. Sonnenschein-van der Voort AM, Jaddoe VW, Raat H, Moll HA, Hofman A, et al. (2012) Fetal and infant growth and asthma symptoms in preschool children: the Generation R Study. Am J Respir Crit Care Med 185: 731–737.
    1. Ortqvist AK, Lundholm C, Carlstrom E, Lichtenstein P, Cnattingius S, et al. (2009) Familial factors do not confound the association between birth weight and childhood asthma. Pediatrics 124: e737–e743.
    1. Escobar GJ, Masaquel AS, Li SX, Walsh EM, Kipnis P (2013) Persistent recurrent wheezing in the fifth year of life after laboratory confirmed, medically attended respiratory syncytial virus infection in infancy. BMC Pediatr 13: 97.
    1. Fauroux B, Gouyon JB, Roze JC, Guillermet-Fromentin C, Glorieux I, et al. (2013) Respiratory morbidity of preterm infants of less than 33 weeks gestation without bronchopulmonary dysplasia: a 12-month follow-up of the CASTOR study cohort. Epidemiol Infect E-pub ahead of print. doi:
    1. Herrera AB, Rodriguez LA, Niederbacher J (2011) Contaminación biológica intradomiciliaria y su relación con síntomas respiratorios indicativos de asma bronquial en preescolares de Bucaramanga, Colombia. Biomédica 31: 357–371.
    1. Nantanda R, Ostergaard MS, Ndeezi G, Tumwine JK (2013) Factors associated with asthma among under-fives in Mulago hospital, Kampala Uganda: a cross sectional study. BMC Pediatr 13: 141.
    1. Rucker G, Schwarzer G, Carpenter JR, Schumacher M (2008) Undue reliance on I(2) in assessing heterogeneity may mislead. BMC Med Res Methodol 8: 79.
    1. Haglund B (2007) Birthweight distributions by gestational age: comparison of LMP-based and ultrasound-based estimates of gestational age using data from the Swedish Birth Registry. Paediatr Perinat Epidemiol 21 (Suppl 2) 72–78.
    1. Been JV, Sheikh A (2013) Gestational age misclassification and its effect on disease outcomes after preterm birth. Eur J Epidemiol 28: 525–526.
    1. Vollsaeter M, Roksund OD, Eide GE, Markestad T, Halvorsen T (2013) Lung function after preterm birth: development from mid-childhood to adulthood. Thorax 68: 767–776.
    1. Goldenberg RL, Culhane JF, Iams JD, Romero R (2008) Epidemiology and causes of preterm birth. Lancet 371: 75–84.
    1. Strand LB, Barnett AG, Tong S (2011) The influence of season and ambient temperature on birth outcomes: a review of the epidemiological literature. Environ Res 111: 451–462.
    1. Culhane JF, Goldenberg RL (2011) Racial disparaties in preterm birth. Semin Perinatol 35: 234–239.
    1. Stocks J, Hislop A, Sonnappa S (2013) Early lung development: lifelong effect on respiratory health and disease. Lancet Respir Med 1: 728–742 doi:
    1. Gantert M, Been JV, Gavilanes AW, Garnier Y, Zimmermann LJ, et al. (2010) Chorioamnionitis: a multiorgan disease of the fetus? J Perinatol 30 (Suppl) S21–S30.
    1. Holgate ST (2012) Innate and adaptive immune responses in asthma. Nat Med 18: 673–683.
    1. Been JV, Rours IG, Kornelisse RF, Jonkers F, de Krijger RR, et al. (2010) Chorioamnionitis alters the response to surfactant in preterm infants. J Pediatr 156: 10–15.
    1. Busse WW, Lemanske RF, Gern JE (2010) Role of viral respiratory infections in asthma and asthma exacerbations. Lancet 376: 826–834.
    1. Lahra MM, Beeby PJ, Jeffery HE (2009) Intrauterine inflammation, neonatal sepsis, and chronic lung disease: a 13-year hospital cohort study. Pediatrics 123: 1314–1319.
    1. Su MW, Tung KY, Liang PH, Tsai CH, Kuo NW, et al. (2012) Gene-gene and gene-environmental interactions of childhood asthma: a multifactor dimension reduction approach. PLoS ONE 7: e30694 doi:
    1. Larsen PS, Kamper-Jorgensen M, Adamson A, Barros H, Bonde JP, et al. (2013) Pregnancy and birth cohort resources in Europe: a large opportunity for aetiological child health research. Paediatr Perinat Epidemiol 27: 393–414.
    1. Blanken MO, Rovers MM, Molenaar JM, Winkler-Seinstra PL, Meijer A, et al. (2013) Respiratory syncytial virus and recurrent wheeze in healthy preterm infants. N Engl J Med 368: 1791–1799.
    1. Alfaleh K, Anabrees J, Bassler D, Al-Kharfi T (2011) Probiotics for prevention of necrotizing enterocolitis in preterm infants. Cochrane Database Syst Rev 2011: CD005496.
    1. Manzoni P, Rinaldi M, Cattani S, Pugni L, Romeo MG, et al. (2009) Bovine lactoferrin supplementation for prevention of late-onset sepsis in very low-birth-weight neonates: a randomized trial. JAMA 302: 1421–1428.

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