Print version ISSN 0365-0596
An. Bras. Dermatol. vol.86 no.3 Rio de Janeiro May/June 2011
Breastfeeding and mucosal and cutaneous colonization by Staphylococcus aureus in atopic children*
Raissa Massaia Londero ChemelloI; Elsa Regina Justo GiuglianiII; Renan Rangel BonamigoIII; Vera Silveira BauerIV; Maria Cristina P. CecconiV; Gladys M. ZubaranVI
IMSc in Epidemiology, Federal University of Rio Grande do Sul (UFRGS) - Porto Alegre (RS), Brazil
IIPhD in Child and Adolescent Health, University of São Paulo (USP) - Technical Area Coordinator of Child Health and Breastfeeding, Ministry of Health (DAPES / SAS / MS) - Porto Alegre (RS), Brazil
IIIMD, PhD Federal University of Rio Grande do Sul (UFRGS) - Coordinator of the Specialization Course in Dermatology and Supervisor of the Medical Residency Program in Dermatology, Federal School of Medical Sciences Foundation of Porto Alegre (FFFCMPA) - Porto Alegre ( RS), Brazil
IVMD - Residency Preceptor, Sanitary Dermatology Outpatient Clinic, State Secretariat of Health of Rio Grande do Sul (SES - RS) - Porto Alegre (RS), Brazil
VTechnician in Human Health and Ecology, State Foundation in Production and Health Research (FEPPS) - Porto Alegre (RS), Brazil
VIPharmacist, Federal University of Santa Maria (UFSM) - Technician, State Foundation in Production and Health Research (FEPPS) - Porto Alegre (RS), Brazil
BACKGROUND: Studies on the effects of breastfeeding on the development of Atopic Dermatitis (AD) have shown controversial results. The importance of this condition deserves further studies; in particular, it remains unclear whether colonization of atopic patients by Staphylococcus aureus (S. aureus) through breastfeeding is relevant to the development of AD.
OBJECTIVE: To examine the potential relation between breastfeeding and colonization by S. aureus in atopic patients.
METHOD: Transversal study of atopic patients, aged from 4 to 24 months, both genders, receiving outpatient care and 72 mothers. Data on infant breastfeeding practices and on clinical-epidemiological profile were registered. Swabs of the infants' nares and skin (cubital fossa) and swabs of the mothers' nares were collected. For univariate analysis, X2 (chi-square) and Fischer Exact's test were used.
RESULTS: Among breastfed children, S. aureus was isolated from 8 (25.8%) infants' nares swabs and from 4 (12.9%) skin swabs. Among not breastfed children, S. aureus was isolated from 10 (20.8%) infants' nares swabs and from 11 (22.9%) skin swabs. Sixteen mothers (22.2%) had S. aureus isolated from their nares swabs. There was no significant association between breastfeeding and S. aureus colonization (child skin and/or nares). However, there was a degree of concordance for S. aureus carriage among mothers and infants. Among 72 pairs, 56 (77.8%) were concordant.
CONCLUSION: Breastfeeding was not associated with S. aureus muco-cutaneous colonization in atopic infants.
Keywords: Breast feeding; Dermatitis, atopic; Staphylococcus aureus
Atopic dermatitis (AD) is one of the most common skin disorders in childhood, occurring in 10 to 30% of children, and which has an upward trend. 1.2 Its etiopathogenesis is complex and multifactorial. Environmental factors such as diet in the first few months of life and skin colonization with Staphylococcus aureus (S. aureus), associated with genetic predisposition, are involved in disease development. 3.4
Some population-based prospective studies have indicated that breastfeeding is a protective factor against AD. 4-7 Exclusive breastfeeding apears to prevent the early development of AD, asthma and allergic rhinitis, as well 5.6 as reduce the risk of AD at 4 years of age 7.
However, some studies have not confirmed this protective effect of breastfeeding. 8-12 Others, paradoxically, suggest that breastfeeding may promote disease development. 9.12 These conflicting findings suggest that the presence of factors not yet fully understood are implicated in the development and progression of AD, such as colonization of the atopic child with bacteria through breastfeeding, among them S. aureus. 13.14
This bacterium has been recognized as the microorganism most frequently associated with AD, playing an important role in the exacerbation and prolongation of this dermatosis. 15-17 Thus, efforts to reduce the mucocutaneous colonization of atopic patients with this bacterium might contribute to the reduction of the signs and symptoms of atopy.
After an electronic search (PubMed and EMBASE) for articles in English published between March/2007 and June/2009, using the key words "(breastfeeding OR breast milk) AND (atopic dermatitis OR eczema)", studies evaluating the association betweeen breastfeeding and colonization with S. aureus of children with atopic dermatitis were not found.
The understanding of a potential association between these factors is a key component in the search for preventive measures that can assist in the treatment of atopic children. This study sought to evaluate a potential association between breastfeeding and colonization with S. aureus of children with AD.
POPULATION AND METHOD
This is a cross-sectional study whose population consisted of breastfed infants diagnosed with atopic dermatitis in the Sanitary Dermatology Outpatient Clinic / State Department of Health, Porto Alegre - Rio Grande do Sul
To estimate the sample size we considered a statistical power of 80%, confidence level of 95%, prevalence of colonization with S. aureus in unexposed children (without breastfeeding) of 20%, and a difference to be detected of 30%. The minimum number of children to be reached was 78.
From September 2007 to December 2008, children between 4 and 24 months of age seen in preassigned shifts and diagnosed with AD were included in the study as long as they did not present any of the following conditions: use of antibiotics or oral corticosteroids 30 days prior to collection of the material for the study; immunosuppression (AIDS, type I diabetes mellitus, chronic use of immunosuppressive drugs); other diseases that compromise the skin barrier, and hospitalization 30 days prior to collection of the material for the study. For analysis purposes, children were classified as breastfed and non-breastfed. Breastfed infants were those who, at the time of data collection, were receiving breast milk, regardless of volume and supplementation with other liquid or solid food. 18
The diagnosis of AD was confirmed by the main researcher (dermatologist) if the child showed symptoms and signs of the disease at clinical examination and/or history of recurrent eczema with typical location. 19, 20 The severity of atopic dermatitis was not considered in the diagnosis.
After the parents or guardians of the child agreed to participate in the study, they completed a questionnaire with demographic and clinical information about the child and its family. Next, the researcher collected material from the nostrils and cubital flexures of the child, where there was no visible lesion, using sterile swabs (moistened with sterile saline solution 0.9%), which were immediately placed in a transport medium with charcoal (Amies) for laboratory analysis. The same procedure was used to collect the nasal swab sample of the child's mother when she was present at the visit.
The material was sent to the Central Laboratory of the State of Rio Grande do Sul, a reference laboratory, within a maximum of 4 hours after collection. The samples were cultured on 5% bovine blood agar and placed in a bacteriological incubator at 37 º C, with readings taken within 24 to 48 hours by two preselected biochemical pharmacists. The catalase test was used to differentiate Streptococcus from Staphylococcus and the coagulase test was performed to differentiate between coagulasenegative and positive Staphylococcus .
Continuous variables with normal distribution were described as mean and standard deviation and the others, as mode or median.
Pearson's Chi-square test was used in the analysis of qualitative variables. Fisher's Exact test was used to evaluate a possible association between the presence of S. aureus in the nose and/or skin of the child and the presence of S. aureus in the maternal nasal cavity. A p-value < 0.05 was considered statistically significant.
The database was created in Excel and the Statistical Package for Social Sciences (SPSS) software, version 13 for Windows, was used in the analysis.
The study protocol was approved by the Ethics and Research Committee of the Public Health School of RS and by the State Foundation in Production and Health Research of RS.
The study included 79 children and 72 mothers, because seven children were brought to the visit by other guardians (father or grandparent). There were no refusals to participate. Most children were in their second year of life, with a mean age of 13.6 ± 6.7 months. Table 1 shows other clinical and epidemiological data from the sample.
The prevalence of colonization with S. aureus in the sample of children studied was 31.6%. Among breastfed children, S. aureus was found in the nasal cavity of 8 (25.8%) and skin (cubital fossa) of 4 (12.9%). Among those who were not receiving breast milk, S. aureus was found in the nasal cavity of 10 (20.8%) and skin of 11 (22.9%). Among the mothers, 16 (22.2%) showed growth of S. aureus in the nasal swab material.
Just over a third of the children (31 - 39.2%) were being breastfed at the time of the study.
There was no significant association between breastfeeding and colonization with S. aureus in the nasal cavity or skin of the child, whose relative prevalence (prevalence ratio) was 0.87 (Table 2). However, there was agreement between colonization with S. aureus in the nasal cavity of the mothers and the nasal cavity and/or skin of their children. Of the 72 pairs, there was agreement (presence or absence) in 56 (77.8%) (Table 3). The concordance between breastfed and non-breastfed children was the same (77.8)%.
The influence of breastfeeding on the development and progression of atopic diseases has been controversial. This study has the merit of perhaps being the first to explore the association between breastfeeding and mucocutaneous colonization with S. aureus of children with AD.
In the general population of children, breastfeeding is suggested as one of the possible factors associated with nasal colonization with S. aureus.13,14,21,22 In this study, however, breastfeeding did not contribute to increase the prevalence of mucocutaneous colonization with S. aureus in the population of atopic children under 2 years old. The low prevalence of colonization with S. aureus in this population (31.6%) compared with the population of other studies, which reported prevalences of up to 90%, draws attention. 1,23,24 Differences in the clinical condition of the children may be involved in these discrepant findings. Unlike the children in this study, children from other studies had severe AD, with great exacerbation of eczema, often needing to be hospitalized. The children in this study had a profile similar to that of the population receiving basic health care: children with less severe disease, mostly with no history of treatment or hospital admission. That would explain why the prevalence of colonization with S. aureus in this study is similar to that found in a lowincome British population of atopic children, who had not received previous treatment or been hospitalized and who had a similar socioeconomic status. 25 The proportion of mothers with positive nasal culture for S. aureus was consistent with the average in the general population observed in other studies. 26.27
Similarly to what has been observed by other authors.13 this study found a positive association between the presence of S. aureus in the maternal nasal mucosa and the skin or nasal mucosa of children, with almost 80% of agreement. Breastfeeding does not appear to have contributed to this finding, given that agreement is similar among breastfed and non-breastfed infants. Considering that this was a cross-sectional study conducted in a single location with a small sample of children seen in a dermatology outpatient clinic with its own characteristics, caution must be exercised in generalizing the findings.
The results of this study should be considered exploratory and potentially hypothesis-generating.
Further studies, preferably with a prospective design, are needed. In addition, more sensitive methods for detection of S. aureus, such as those used in molecular microbiology (polymerase chain reaction and pulsed field gel electrophoresis) could be useful to prove that the S. aureus present in both mother and child has the same origin.
This study evaluated the possible role of breastfeeding in the colonization with S. aureus of children with AD. No association was found between breastfeeding and colonization with S. aureus. However, we found that of the 16 mothers (22.2% of total sample) who were positive for S. aureus in nasal swab, only five had children who were negative for S. aureus (swab of the nasal cavity or the skin with visible lesion). Moreover, among the 56 mothers (77.8% of total sample) with negative results, 45 had children with negative results as well (nasal cavity or skin without visible lesion). Thus, the presence of S. aureus in the maternal nasal cavity was associated with the presence of the bacteria in the nasal cavity or skin of the patient. Questions such as whether the environment and/or genetics of mother and child have some influence, or the role that breastfeeding plays in this scenario, are potential generators of hypotheses.
In conclusion, due to the important and controversial relationship between colonization with S. aureus, breastfeeding and AD, future research is appropriate. The understanding of a potential association between these factors - not yet reported in the literature - is a key component in the search for preventive measures that will assist in the future treatment of patients with AD.
1. Bieber T. Atopic dermatitis. N Engl J Med. 2008;358:1483-94. [ Links ]
2. Addor FAS, Aoki V. Barreira cutânea na dermatite atópica. 2010;85:184-94. [ Links ]
3. Ellis C, Luger T, Abeck D, Allen R, Graham-Brown RA, De Prost Y, et al. International Consensus Conference on Atopic Dermatitis II (ICCAD II): clinical update and current treatment strategies. Br J Dermatol. 2003;148(Suppl 63):3-10. [ Links ]
4. Greer FR, Sicherer SH, Burks AW; American Academy of Pediatrics Committee on Nutrition; American Academy of Pediatrics Section on Allergy and Immunology. Effects of early nutritional interventions on the development of atopic disease in infants and children: the role of maternal dietary restriction, breastfeeding, timing of introduction of complementary foods, and hydrolyzed formulas. Pediatrics. 2008;121:183-91. [ Links ]
5. Gdalevich M, Mimouni D, David M, Mimoumi M. Breast-feeding and the onset of atopic dermatitis in childhood: a systematic review and meta-analysis of prospective studies. J Am Acad Dermatol. 2001;45:520-7. [ Links ]
6. Kull I, Wickman M, Lilja G, Nordvall SL, Pershagen G. Breast feeding and allergic diseases in infants-a prospective birth cohort study. Arch Dis Child. 2002;87:478-81. [ Links ]
7. Kull I, Bohme M, Wahlgren C, Nordvall L, Pershagen G, Wickman M. Breastfeeding reduces the risk for childhood eczema. J Allergy Clin Immunol. 2005;116:657-61. [ Links ]
8. Friedman NJ, Zeiger RS. The role of breast-feeding in the development of allergies and asthma. J Allergy Clin Immunol. 2005;115:1238-48. [ Links ]
9. Mihrshahi S, Ampon R, Webb K, Almqvist C, Kemp AS, Hector D, et al. The association between infant feeding practices and subsequent atopy among children with a family history of asthma. Clin Exp Allergy. 2007;37:671-9. [ Links ]
10. Ludvigsson JF, Mostrom M, Ludvigsson J, Duchen K. Exclusive breastfeeding and risk of atopic dermatitis in some 8300 infants. Pediatr Allergy Immunol. 2005;16:201-8. [ Links ]
11. Elliott L, Henderson J, Northstone K, Chiu G, Dunson D, London S. Prospective study of breast-feeding in relation to wheeze, atopy, and bronchial hyperresponsiveness in the Avon Longitudinal Study of Parents and Children (ALSPAC). J Allergy Clin Immunol. 2008;122:49-54. e1-3. [ Links ]
12. Pesonen M, Kallio MJT, Ranki A, Simes MA. Prolonged exclusive breastfeeding is associated with increased atopic dermatitis: a prospective follow-up study of unselected healthy newborns from birth to age 20 years. Clin Exp Allergy. 2006;36:1011-8. [ Links ]
13. Peacock SJ, Justice A, Griffiths D, de Silva GD, Kantzanou MN, Crook D, et al. Determinants of acquisition and carriage of Staphylococcus aureus in infancy. J Clin Microbiol. 2003;41:5718-25. [ Links ]
14. Kawada M, Okuzumi K, Hitomi S, Sugishita C. Transmission of Staphylococcus aureus between healthy, lactating mothers and their infants by breastfeeding. J Hum Lact. 2003;19:411-17. [ Links ]
15. Leung DY. Atopic dermatitis and the immune system: the role of superantigens and bacteria. J Am Acad Dermatol. 2001;45(1 Suppl):S13-6. [ Links ]
16. Morishita Y, Tada J, Sato A, Toi Y, Kanzaki H, Akiyama H, et al. Possible influences of Staphylococcus aureus on atopic dermatitis-- the colonizing features and the effects of staphylococcal enterotoxins. Clin Exp Allergy. 1999;29:1110-7. [ Links ]
17. Gill S. An overview of atopic eczema in children: a significant disease. Br J Nurs. 2006;15:494-9. [ Links ]
18. Hanifin JM, Rajka G. Diagnostic Feature of Atopic Dermatitis. Acta Derm Venereol (Stockh). 1980;92(Suppl 190):44-7. [ Links ]
19. Williams HC, Jburney PG, Pembroke AC, Hay RJ. The U.K. Working Party's Diagnostic Criteria for Atopic Dermatitis. III. Independent hospital validation. Br J Dermatol. 1994;131:406-16. [ Links ]
20. World Health Organization. Indicators for assessing infant and young child feeding practices. Conclusions of a consensus meeting held 6-8 November 2007. Washington D.C., 2007. [ Links ]
21. Le Thomas I, Mariani-Kurkdjian P, Collignon A, Gravet A, Clermont O, Brahimi N, et al. Breast milk transmission of a Panton-Valentine leukocidin-producing Staphylococcus aureus strain causing infantile pneumonia. J Clin Microbiol. 2001;39:728-9. [ Links ]
22. Amir L. Breastfeeding and Staphylococcus aureus: three case reports. Breastfeed Rev. 2002;10:15-8. [ Links ]
23. Breuer K, Kapp A, Werfel T. Bacterial infections and atopic dermatitis. Allergy. 2001;56:1034-41. [ Links ]
24. Birnie AJ, Bath-Hextall FJ, Ravenscroft JC, Williams HC. Interventions to reduce Staphylococcus aureus in the management of atopic eczema. Cochrane Database Syst Rev. 2008:CD003871. [ Links ]
25. Goodyear HM, Watson PJ, Egan SA, Price EH, Kenny PA, Harper JI. Skin microflora of atopic eczema in first time hospital attenders. Clin Exp Dermatol. 1993;18:300-4. [ Links ]
26. Kluytmans J, van Belkum A, Verbrugh H. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev. 1997;10:505-20. [ Links ]
27. Amir LH, Garland SM, Lumley J. A case-control study of mastitis: nasal carriage of Staphylococcus aureus. BMC Fam Pract. 2006;7:57. [ Links ]
Mailing address: Received on 18.07.2010. * Work conducted at the Sanitary Dermatology Outpatient Clinic of Porto Alegre (ADS - RS) and Central Laboratory of Public Health of Rio Grande do Sul (LACEN - RS) - Porto Alegre (RS), Brazil.
Raissa Massaia Londero Chemello
Rua Mostardeiro, 157/401
90430-001 Porto Alegre - RS
Approved by the Advisory Board and accepted for publication on 03.08.10.
Conflict of interest: None
Financial funding: None
Received on 18.07.2010.
* Work conducted at the Sanitary Dermatology Outpatient Clinic of Porto Alegre (ADS - RS) and Central Laboratory of Public Health of Rio Grande do Sul (LACEN - RS) - Porto Alegre (RS), Brazil.