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© Thomson Reuters, Journal Citation Reports, 2016

Allergol Immunopathol (Madr) 2011;39:315-7 - DOI: 10.1016/j.aller.2011.09.001
Editorial
Breastfeeding and asthma: Where are we?
R.T. Cohen??,
Section of Pulmonology and Allergy, Dept. of Pediatrics, St. Christopher's Hospital for Children, Drexel University College of Medicine, Philadelphia, PA, USA
J.C. Celedón
Division of Pediatric Pulmonary Medicine, Allergy and Immunology, Dept. of Pediatrics, Children's Hospital of Pittsburgh of UPMC, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA

Asthma and atopic diseases are major public health problems worldwide.1 Identifying modifiable factors associated with the pathogenesis of asthma, allergies, and eczema is important for developing targeted interventions for the prevention of these conditions, particularly among children at highest risk. The relation between breastfeeding and atopy has long been a subject of both interest2 and debate.3 In describing a “golden jubilee of controversy” in 1988, Kramer proposed 12 methodological and biological criteria to evaluate studies of breastfeeding and allergy or asthma, including (but not limited to): non-reliance on late maternal recall of breastfeeding, duration and exclusivity of breastfeeding, strict diagnostic criteria of the outcome, ascertainment of severity, age of onset, and risk of the outcome; and assessment of dose-response effects.4

In the current issue of Allergologia et immunopathologia, Bjorksten et al. report a lack of association between breastfeeding and current wheeze, current rhinoconjunctivitis or current eczema among children of school age in Phase III of ISAAC (the International Study of Asthma and Allergy in Childhood).5 The authors noted an inverse association between breastfeeding and symptoms of severe rhinoconjunctivitis or severe eczema.5 The strengths of this study include its large global sample size (206,453 children from 32 countries including 103,716 children with complete data) from a school-based random sample6 as well as the extent to which the ISAAC questionnaires have been translated into multiple languages and validated around the world.7,8 The fact that the multivariable models included adjustment for maternal smoking during infancy is also important, as maternal smoking may modify any effects of breast feeding on risk of lower respiratory tract infections and asthma.9–12

Unfortunately, several elements of the study design prevented the authors from definitively putting this controversy to rest. First, as mentioned by the authors, data on breastfeeding were limited to a yes/no response to the question “Was your child breast fed?” Such a limited ascertainment of breastfeeding precludes any ability to identify a dose-response or a threshold of exposure necessary to detect an effect. Does exclusive breast feeding confer more protection compared to breastfeeding supplemented with formula? Is a specific duration (4 months being the standard in most studies) required for a beneficial impact? Perhaps. Second, family history of atopy was not included. As multiple studies have asserted13,14 there may be a differential effect of breastfeeding on the risk of developing asthma and/or allergies depending on whether or not the mother herself is atopic.

In a prospective birth cohort of 2602 children in Western Australia, exclusive breastfeeding for at least 4 months was associated with a decreased risk of asthma at age six years, regardless of maternal history of asthma.15 Data from over 4000 children in a prospective birth cohort in Sweden suggest that the association between breastfeeding and asthma was not as strong in those with a family history of allergic disease (OR 0.73, 95% CI 0.43–1.20) as in those without a family history (OR 0.58, 95% CI 0.38–0.88).16 In another study in Tucson, AZ, USA, breastfeeding was inversely associated with recurrent wheeze at age two years (regardless of maternal history of atopy) but positively associated with asthma at age 6 years among children with maternal history of asthma (asthma prevalence among those with: exclusive BF>4 months=46%, BF<4 months=23.5%, never BF 9.1%, p<0.005).14 Furthermore, data from the same cohort show that at age 16 years, children of asthmatic mothers who were exclusively BF for >4 months had lower lung function on spirometry than those who were not BF.17 In contrast, the Isle of Wight prospective birth cohort showed that exclusive breastfeeding for >4 months was associated with increased lung function (higher FVC, FEV1, and peak expiratory flow rates) at age 10 years, regardless of maternal history of asthma and/or atopy.18

Why have there been such disparate findings across studies? What are the potential mechanisms that underlie both the protective effects of breastfeeding seen in some cohorts and the increased risk associated with breastfeeding demonstrated in others? The answers to these questions may depend on individual level factors rather than what can be assessed in large population-based observational studies. For example, data from intervention trials suggest that food allergen avoidance (including dairy, egg, nut, soy, etc.) by lactating mothers of children at high risk for atopy may reduce antigen exposure for those infants and thus be beneficial in reducing later risk of food allergy and atopic eczema.19,20 In addition, Verhasselt et al. found that compared to mice breastfed by unexposed mothers, mice breastfed by mothers with exposure to airborne allergen (ovalbumin) during lactation developed antigen-specific tolerance and reduced airway hyper-reactivity and allergic inflammation in response to ovalbumin challenge.21 In addition to effects of antigen exposure, investigators have looked at other aspects of breast milk composition. Studies focusing on long chain n-3 fatty acids (LCFA, which may have immunomodulatory effects) have found that maternal dietary intake has little impact on LCFA content in breast milk22; that there are minimal differences in LCFA content of breast milk between allergic and non-allergic mothers23,24; and that higher LCFA levels in breast milk may actually be associated with increased rather than decreased risk of atopy in high-risk infants.24 From a methodological standpoint, some have argued that observational studies showing an increased risk of allergy among exclusively breastfed infants may be influenced by “reverse causation” (an increased tendency of mothers of high-risk children to exclusively breastfeed their children for longer duration because of well-publicised perceived protective benefits of breastfeeding).25,26

Future studies in this field should include as detailed a prospective ascertainment of breastfeeding as possible (including information on exclusivity and duration), collection of breast milk for composition analysis (including antigens, immunological factors, and potentially toxic exposures), ascertainment of potential mediators of effects on asthma (including viral infections during early childhood and environmental tobacco smoke exposure)9–11 and clearly defined outcomes based on objective diagnostic criteria (e.g., allergy markers, lung function measures) Ongoing and future clinical trials of early versus delayed introduction of foodstuff during breast feeding should help elucidate the relation between breastfeeding and asthma or allergies.

References
1
N. Pearce,N. Ait-Khaled,R. Beasley,J. Mallol,U. Keil,E. Mitchell
Worldwide trends in the prevalence of asthma symptoms: phase III of the International Study of Asthma and Allergies in Childhood ISAAC
2
U.M. Saarinen,M. Kajosaari,A. Backman,M.A. Siimes
Prolonged breast-feeding as prophylaxis for atopic disease
Lancet, 2 (1979), pp. 163-166
3
J.M. Duncan,M.R. Sears
Breastfeeding and allergies: time for a change in paradigm?
Curr Opin Allergy Clin Immunol, 8 (2008), pp. 398-405 http://dx.doi.org/10.1097/ACI.0b013e32830d82ed
4
M.S. Kramer
Does breast feeding help protect against atopic disease? Biology, methodology, and a golden jubilee of controversy
J Pediatr, 112 (1988), pp. 181-190
5
Bjorksten B, Ait-Khaled N, Innes Asher M, Clayton TO, Robertson C. Global analysis of breast feeding and risk of symptoms of asthma, rhinoconjunctivitis and eczema in 6-7 year old children: ISAAC Phase Three. Allergol Immunopathol 2011.
6
M.I. Asher,U. Keil,H.R. Anderson,R. Beasley,J. Crane,F. Martinez
International study of asthma and allergies in childhood (ISAAC): rationale and methods
Eur Respir J, 8 (1995), pp. 483-491
7
P. Ellwood,H. Williams,N. Ait-Khaled,B. Bjorksten,C. Robertson
Translation of questions: the international study of asthma and allergies in childhood (ISAAC) experience
Int J Tuberc Lung Dis, 13 (2009), pp. 1174-1182
8
C. Mata Fernandez,M. Fernandez-Benitez,M. Perez Miranda,F. Guillen Grima
Validation of the Spanish version of the Phase III ISAAC questionnaire on asthma
J Investig Allergol Clin Immunol, 15 (2005), pp. 201-210
9
P. Nafstad,J.J. Jaakkola,J.A. Hagen,G. Botten,J. Kongerud
Breastfeeding, maternal smoking and lower respiratory tract infections
Eur Respir J, 9 (1996), pp. 2623-2629
10
F. Ladomenou,J. Moschandreas,A. Kafatos,Y. Tselentis,E. Galanakis
Protective effect of exclusive breastfeeding against infections during infancy: a prospective study
Arch Dis Child, 95 (2003), pp. 1004-1008 http://dx.doi.org/10.1136/adc.2009.169912
11
W. Karmaus,A.L. Dobai,I. Ogbuanu,S.H. Arshard,S. Matthews,S. Ewart
Long-term effects of breastfeeding, maternal smoking during pregnancy, and recurrent lower respiratory tract infections on asthma in children
12
H.T. Guedes,L.S. Souza
Exposure to maternal smoking in the first year of life interferes in breast-feeding protective effect against the onset of respiratory allergy from birth to 5 yr
Pediatr Allergy Immunol, 20 (2009), pp. 30-34 http://dx.doi.org/10.1111/j.1399-3038.2007.00710.x
13
M.R. Sears,J.M. Greene,A.R. Willan,D.R. Taylor,E.M. Flannery,J.O. Cowan
Long-term relation between breastfeeding and development of atopy and asthma in children and young adults: a longitudinal study
14
A.L. Wright,C.J. Holberg,L.M. Taussig,F.D. Martinez
Factors influencing the relation of infant feeding to asthma and recurrent wheeze in childhood
Thorax, 56 (2001), pp. 192-197
15
W.H. Oddy,J.K. Peat,N.H. de Klerk
Maternal asthma, infant feeding, and the risk of asthma in childhood
J Allergy Clin Immunol, 110 (2002), pp. 65-67
16
I. Kull,C. Almqvist,G. Lilja,G. Pershagen,M. Wickman
Breast-feeding reduces the risk of asthma during the first 4 years of life
J Allergy Clin Immunol, 114 (2004), pp. 755-760 http://dx.doi.org/10.1016/j.jaci.2004.07.036
17
T.W. Guilbert,D.A. Stern,W.J. Morgan,F.D. Martinez,A.L. Wright
Effect of breastfeeding on lung function in childhood and modulation by maternal asthma and atopy
Am J Respir Crit Care Med, 176 (2007), pp. 843-848 http://dx.doi.org/10.1164/rccm.200610-1507OC
18
I.U. Ogbuanu,W. Karmaus,S.H. Arshad,R.J. Kurukulaaratchy,S. Ewart
Effect of breastfeeding duration on lung function at age 10 years: a prospective birth cohort study
19
S.H. Arshad,B. Bateman,S.M. Matthews
Primary prevention of asthma and atopy during childhood by allergen avoidance in infancy: a randomised controlled study
Thorax, 58 (2003), pp. 489-493
20
A. Host,S. Halken,A. Muraro,S. Dreborg,B. Niggemann,R. Aalberse
Dietary prevention of allergic diseases in infants and small children
Pediatr Allergy Immunol, 19 (2008), pp. 1-4 http://dx.doi.org/10.1111/j.1399-3038.2008.00762.x
21
V. Verhasselt,V. Milcent,J. Cazareth,A. Kanda,S. Fleury,D. Dombrowicz
Breast milk-mediated transfer of an antigen induces tolerance and protection from allergic asthma
Nat Med, 14 (2008), pp. 170-175 http://dx.doi.org/10.1038/nm1718
22
S. Johansson,A.E. Wold,A.S. Sandberg
Low breast milk levels of long-chain n-3 fatty acids in allergic women, despite frequent fish intake
Clin Exp Allergy, 41 (2003), pp. 505-515 http://dx.doi.org/10.1111/j.1365-2222.2010.03678.x
23
A. Wijga,A.C. Houwelingen,H.A. Smit,M. Kerkhof,A.P. Vos,H.J. Neijens
Fatty acids in breast milk of allergic and non-allergic mothers: The PIAMA birth cohort study
Pediatr Allergy Immunol, 14 (2003), pp. 156-162
24
R.M. Stoney,R.K. Woods,C.S. Hosking,D.J. Hill,M.J. Abramson,F.C. Thien
Maternal breast milk long-chain n-3 fatty acids are associated with increased risk of atopy in breastfed infants
Clin Exp Allergy, 34 (2004), pp. 194-200
25
T. Kusunoki,T. Morimoto,R. Nishikomori,T. Yasumi,T. Heike,K. Mukaida
Breastfeeding and the prevalence of allergic diseases in schoolchildren: does reverse causation matter?
Pediatr Allergy Immunol, 21 (2008), pp. 60-66 http://dx.doi.org/10.1111/j.1399-3038.2009.00982.x
26
C.J. Lodge,A.J. Lowe,S.C. Dharmage
Is reverse causation responsible for the link between duration of breastfeeding and childhood asthma?
Am J Respir Crit Care Med, 178 (2008), pp. 994 http://dx.doi.org/10.1164/ajrccm.178.9.994

Sources of support: Grant HL079966 from the U.S. National Institutes of Health.

Corresponding author. (R.T. Cohen robyn.cohen@drexelmed.edu)
Copyright © 2011. SEICAP