The skin microbiome in the first year of life and its association with atopic dermatitis.
atopic dermatitis
cohort study
infancy
microbiome
skin
Journal
Allergy
ISSN: 1398-9995
Titre abrégé: Allergy
Pays: Denmark
ID NLM: 7804028
Informations de publication
Date de publication:
07 2023
07 2023
Historique:
revised:
14
12
2022
received:
24
07
2022
accepted:
04
01
2023
medline:
3
7
2023
pubmed:
14
2
2023
entrez:
13
2
2023
Statut:
ppublish
Résumé
Early-life microbial colonization of the skin may modulate the immune system and impact the development of atopic dermatitis (AD) and allergic diseases later in life. To address this question, we assessed the association between the skin microbiome and AD, skin barrier integrity and allergic diseases in the first year of life. We further explored the evolution of the skin microbiome with age and its possible determinants, including delivery mode. Skin microbiome was sampled from the lateral upper arm on the first day of life, and at 3, 6, and 12 months of age. Bacterial communities were assessed by 16S rRNA gene amplicon sequencing in 346 infants from the PreventADALL population-based birth cohort study, representing 970 samples. Clinical investigations included skin examination and skin barrier function measured as trans-epidermal water loss (TEWL) at the site and time of microbiome sampling at 3, 6, and 12 months. Parental background information was recorded in electronic questionnaires, and delivery mode (including vaginal delivery (VD), VD in water, elective caesarean section (CS) and emergency CS) was obtained from maternal hospital charts. Strong temporal variations in skin bacterial community composition were found in the first year of life, with distinct patterns associated with different ages. Confirming our hypothesis, skin bacterial community composition in the first year of life was associated with skin barrier integrity and later onsets of AD. Delivery mode had a strong impact on the microbiome composition at birth, with each mode leading to distinct patterns of colonization. Other possible determinants of the skin microbiome were identified, including environmental and parental factors as well as breastfeeding. Skin microbiome composition during infancy is defined by age, transiently influenced by delivery mode as well as environmental, parental factors and breastfeeding. The microbiome is also associated with skin barrier integrity and the onset of AD.
Sections du résumé
BACKGROUND
Early-life microbial colonization of the skin may modulate the immune system and impact the development of atopic dermatitis (AD) and allergic diseases later in life. To address this question, we assessed the association between the skin microbiome and AD, skin barrier integrity and allergic diseases in the first year of life. We further explored the evolution of the skin microbiome with age and its possible determinants, including delivery mode.
METHODS
Skin microbiome was sampled from the lateral upper arm on the first day of life, and at 3, 6, and 12 months of age. Bacterial communities were assessed by 16S rRNA gene amplicon sequencing in 346 infants from the PreventADALL population-based birth cohort study, representing 970 samples. Clinical investigations included skin examination and skin barrier function measured as trans-epidermal water loss (TEWL) at the site and time of microbiome sampling at 3, 6, and 12 months. Parental background information was recorded in electronic questionnaires, and delivery mode (including vaginal delivery (VD), VD in water, elective caesarean section (CS) and emergency CS) was obtained from maternal hospital charts.
RESULTS
Strong temporal variations in skin bacterial community composition were found in the first year of life, with distinct patterns associated with different ages. Confirming our hypothesis, skin bacterial community composition in the first year of life was associated with skin barrier integrity and later onsets of AD. Delivery mode had a strong impact on the microbiome composition at birth, with each mode leading to distinct patterns of colonization. Other possible determinants of the skin microbiome were identified, including environmental and parental factors as well as breastfeeding.
CONCLUSION
Skin microbiome composition during infancy is defined by age, transiently influenced by delivery mode as well as environmental, parental factors and breastfeeding. The microbiome is also associated with skin barrier integrity and the onset of AD.
Substances chimiques
RNA, Ribosomal, 16S
0
Water
059QF0KO0R
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1949-1963Informations de copyright
© 2023 The Authors. Allergy published by European Academy of Allergy and Clinical Immunology and John Wiley & Sons Ltd.
Références
Tsakok T, Woolf R, Smith CH, Weidinger S, Flohr C. Atopic dermatitis: the skin barrier and beyond. Br J Dermatol. 2019;180(3):464-474.
Berents TL, Lødrup Carlsen KC, Mowinckel P, et al. Transepidermal water loss in infancy associated with atopic eczema at 2 years of age: a population-based cohort study. Br J Dermatol. 2017;177(3):e35-e37.
Rehbinder EM, Advocaat Endre KM, Lødrup Carlsen KC, et al. Predicting skin barrier dysfunction and atopic dermatitis in early infancy. J Allergy Clin Immunol Pract. 2020;8(2):664-673.e5.
Zheng D, Liwinski T, Elinav E. Interaction between microbiota and immunity in health and disease. Cell Res. 2020;30:492-506.
Ubags ND, Trompette A, Pernot J, et al. Microbiome-induced antigen-presenting cell recruitment coordinates skin and lung allergic inflammation. J Allergy Clin Immunol. 2021;147(3):1049-1062.e7.
Han P, Gu JQ, Li LS, et al. The association between intestinal bacteria and allergic diseases-cause or consequence? Front Cell Infect Microbiol. 2021;11:650893.
Chen P, He G, Qian J, Zhan Y, Xiao R. Potential role of the skin microbiota in inflammatory skin diseases. J Cosmet Dermatol. 2021;20(2):400-409.
Renz H, Holt PG, Inouye M, Logan AC, Prescott SL, Sly PD. An exposome perspective: early-life events and immune development in a changing world. J Allergy Clin Immunol. 2017;140(1):24-40.
Narla S, Silverberg JI. The role of environmental exposures in atopic dermatitis. Curr Allergy Asthma Rep. 2020;20(12):74.
Combellick JL, Shin H, Shin D, et al. Differences in the fecal microbiota of neonates born at home or in the hospital. Sci Rep. 2018;8(1):15660.
Fehervary P, Lauinger-Lörsch E, Hof H, Melchert F, Bauer L, Zieger W. Water birth: microbiological colonisation of the newborn, neonatal and maternal infection rate in comparison to conventional bed deliveries. Arch Gynecol Obstet. 2004;270(1):6-9.
Kong HH, Oh J, Deming C, et al. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res. 2012;22(5):850-859.
Khadka VD, Key FM, Romo-González C, et al. The skin microbiome of patients with atopic dermatitis normalizes gradually during treatment. Front Cell Infect Microbiol. 2021;11:720674.
Kwon S, Choi JY, Shin JW, et al. Changes in Lesional and non-lesional skin microbiome during treatment of atopic dermatitis. Acta Derm Venereol. 2019;99(3):284-290.
Callewaert C, Nakatsuji T, Knight R, et al. IL-4Rα blockade by Dupilumab decreases Staphylococcus aureus colonization and increases microbial diversity in atopic dermatitis. J Invest Dermatol. 2020;140(1):191-202.e7.
Lossius AH, Sundnes O, Ingham AC, et al. Shifts in the skin microbiota after UVB treatment in adult atopic dermatitis. DRM. 2022;238(1):109-120.
Kennedy EA, Connolly J, Hourihane JO, et al. Skin microbiome before development of atopic dermatitis: early colonization with commensal staphylococci at 2 months is associated with a lower risk of atopic dermatitis at 1 year. J Allergy Clin Immunol. 2017;139(1):166-172.
Fölster-Holst R, Reimer R, Neumann C, et al. Comparison of epidermal barrier integrity in adults with classic atopic dermatitis, atopic Prurigo and non-atopic Prurigo Nodularis. Biology (Basel). 2021;10(10):1008.
Lødrup Carlsen KC, Rehbinder EM, Skjerven HO, et al. Preventing atopic dermatitis and ALLergies in children-the PreventADALL study. Allergy. 2018;73(10):2063-2070.
Skjerven HO, Rehbinder EM, Vettukattil R, et al. Skin emollient and early complementary feeding to prevent infant atopic dermatitis (PreventADALL): a factorial, multicentre, cluster-randomised trial. Lancet. 2020;395(10228):951-961.
Skjerven HO, Lie A, Vettukattil R, et al. Early food intervention and skin emollients to prevent food allergy in young children (PreventADALL): a factorial, multicentre, cluster-randomised trial. Lancet. 2022;399(10344):2398-2411.
Dotterud LK, Odland JØ, Falk ES. Atopic dermatitis and respiratory symptoms in Russian and northern Norwegian school children: a comparison study in two arctic areas and the impact of environmental factors. J Eur Acad Dermatol Venereol. 2004;18(2):131-136.
Carson CG, Rasmussen MA, Thyssen JP, Menné T, Bisgaard H. Clinical presentation of atopic dermatitis by filaggrin gene mutation status during the first 7 years of life in a prospective cohort study. PLoS One. 2012;7(11):e48678.
Williams HC, Burney 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(3):406-416.
Hanifin JM, Rajka G. Diagnostic features of atopic dermatitis. Acta Derm Venereol. 1980;92:44-47.
Endre KMA, Landrø L, LeBlanc M, et al. Diagnosing atopic dermatitis in infancy using established diagnostic criteria: a cohort study. Br J Dermatol. 2022;186(1):50-58.
Rapin A, Pattaroni C, Marsland BJ, Harris NL. Microbiota analysis using an Illumina MiSeq platform to sequence 16 S rRNA genes. Curr Protoc Mouse Biol. 2017;7(2):100-129.
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581-583.
Wang W, Chen EZ, Li H. Truncated rank-based tests for two-part models with excessive zeros and applications to microbiome data [Internet]. arXiv. 2021. http://arxiv.org/abs/2110.05368
Lê Cao KA, Boitard S, Besse P. Sparse PLS discriminant analysis: biologically relevant feature selection and graphical displays for multiclass problems. BMC Bioinformatics. 2011;12(1):253.
Capone KA, Dowd SE, Stamatas GN, Nikolovski J. Diversity of the human skin microbiome early in life. J Invest Dermatol. 2011;131(10):2026-2032.
Pammi M, O'Brien JL, Ajami NJ, Wong MC, Versalovic J, Petrosino JF. Development of the cutaneous microbiome in the preterm infant: a prospective longitudinal study. PLoS One. 2017;12(4):e0176669.
Gaitanis G, Tsiouri G, Spyridonos P, et al. Variation of cultured skin microbiota in mothers and their infants during the first year postpartum. Pediatr Dermatol. 2019;36(4):460-465.
Glatz M, Jo JH, Kennedy EA, et al. Emollient use alters skin barrier and microbes in infants at risk for developing atopic dermatitis. PLoS One. 2018;13(2):e0192443.
Łoś-Rycharska E, Gołębiewski M, Sikora M, et al. A combined analysis of gut and skin microbiota in infants with food allergy and atopic dermatitis: a pilot study. Nutrients. 2021;13(5):1682.
Shi B, Bangayan NJ, Curd E, et al. The skin microbiome is different in pediatric versus adult atopic dermatitis. J Allergy Clin Immunol. 2016;138(4):1233-1236.
Byrd AL, Deming C, Cassidy SKB, et al. Staphylococcus aureus and Staphylococcus epidermidis strain diversity underlying pediatric atopic dermatitis. Sci Transl Med. 2017;9(397):eaal4651.
Ramadan M, Solyman S, Yones M, Abdallah Y, Halaby H, Hanora A. Skin microbiome differences in atopic dermatitis and healthy controls in Egyptian children and adults, and association with serum immunoglobulin E. Omics. 2019;23(5):247-260.
Lack G. Update on risk factors for food allergy. J Allergy Clin Immunol. 2012;129(5):1187-1197.
Roduit C, Wohlgensinger J, Frei R, et al. Prenatal animal contact and gene expression of innate immunity receptors at birth are associated with atopic dermatitis. J Allergy Clin Immunol. 2011;127(1):179-185.e1.
Gołębiewski M, Łoś-Rycharska E, Sikora M, Grzybowski T, Gorzkiewicz M, Krogulska A. Mother's Milk microbiome shaping fecal and skin microbiota in infants with food allergy and atopic dermatitis: a pilot analysis. Nutrients. 2021;13(10):3600.
Dominguez-Bello MG, Costello EK, Contreras M, 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(26):11971-11975.
Chu DM, Ma J, Prince AL, Antony KM, Seferovic MD, Aagaard KM. Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nat Med. 2017;23(3):314-326.
Rutayisire E, Huang K, Liu Y, Tao F. The mode of delivery affects the diversity and colonization pattern of the gut microbiota during the first year of infants' life: a systematic review. BMC Gastroenterol. 2016;16(1):86.
Azad MB, Konya T, Maughan H, et al. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ. 2013;185(5):385-394.
Rehbinder EM, Lødrup Carlsen KC, Staff AC, et al. Is amniotic fluid of women with uncomplicated term pregnancies free of bacteria? Am J Obstet Gynecol. 2018;219(3):289.e1-289.e12.
Chang HY, Suh DI, Yang SI, et al. Prenatal maternal distress affects atopic dermatitis in offspring mediated by oxidative stress. J Allergy Clin Immunol. 2016;138(2):468-475.e5.
Lee SY, Kang MJ, Kwon SO, et al. Prenatal maternal anxiety related with dietary pattern may promote atopic dermatitis in offspring through the alteration of gut microbiota. J Allergy Clin Immunol. 2019;143(2):AB133.
Zochowski MK, Kolenic GE, Zivin K, et al. Trends In primary cesarean section rates among women with and without perinatal mood and anxiety disorders. Health Aff (Millwood). 2021;40(10):1585-1591.
Seite S, Flores GE, Henley JB, et al. Microbiome of affected and unaffected skin of patients with atopic dermatitis before and after emollient treatment. J Drugs Dermatol. 2014;13(11):1365-1372.
Xu Z, Liu X, Niu Y, et al. Skin benefits of moisturising body wash formulas for children with atopic dermatitis: a randomised controlled clinical study in China. Australas J Dermatol. 2020;61(1):e54-e59.
Weidinger S, Beck LA, Bieber T, Kabashima K, Irvine AD. Atopic dermatitis. Nat Rev Dis Primers. 2018;4(1):1.
Hoyer A, Rehbinder EM, Färdig M, et al. Filaggrin mutations in relation to skin barrier and atopic dermatitis in early infancy. Br J Dermatol. 2022;186(3):544-552.