Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis

Heidi H. Kong, Julia Oh, Clay Deming, Sean Conlan, Elizabeth A. Grice, Melony A. Beatson, Effie Nomicos, Eric Polley, Hirsh D. Komarow, Jim Mullikin, Jim Thomas, Robert Blakesley, Alice Young, Grace Chu, Colleen Ramsahoye, Sean Lovett, Joel Han, Richelle Legaspi, Christina Sison, Casandra MontemayorMichael Gregory, April Hargrove, Taccara Johnson, Nancy Riebow, Brian Schmidt, Betsy Novotny, Jyoti Gupta, Betty Benjamin, Shelise Brooks, Holly Coleman, Shi Ling Ho, Karen Schandler, Mal Stantripop, Quino Maduro, Gerry Bouffard, Mila Dekhtyar, Xiaobin Guan, Cathy Masiello, Baishali Maskeri, Jenny McDowell, Morgan Park, Meg Vemulapalli, Patrick R. Murray, Maria L. Turner, Julia A. Segre

Research output: Contribution to journalArticle

609 Citations (Scopus)

Abstract

Atopic dermatitis (AD) has long been associated with Staphylococcus aureus skin colonization or infection and is typically managed with regimens that include antimicrobial therapies. However, the role of microbial communities in the pathogenesis of AD is incompletely characterized. To assess the relationship between skin microbiota and disease progression, 16S ribosomal RNA bacterial gene sequencing was performed on DNA obtained directly from serial skin sampling of children with AD. The composition of bacterial communities was analyzed during AD disease states to identify characteristics associated with AD flares and improvement post-treatment. We found that microbial community structures at sites of disease predilection were dramatically different in AD patients compared with controls. Microbial diversity during AD flares was dependent on the presence or absence of recent AD treatments, with even intermittent treatment linked to greater bacterial diversity than no recent treatment. Treatment-associated changes in skin bacterial diversity suggest that AD treatments diversify skin bacteria preceding improvements in disease activity. In AD, the proportion of Staphylococcus sequences, particularly S. aureus, was greater during disease flares than at baseline or post-treatment, and correlated with worsened disease severity. Representation of the skin commensal S. epidermidis also significantly increased during flares. Increases in Streptococcus, Propionibacterium, and Corynebacterium species were observed following therapy. These findings reveal linkages between microbial communities and inflammatory diseases such as AD, and demonstrate that as compared with culture-based studies, higher resolution examination of microbiota associated with human disease provides novel insights into global shifts of bacteria relevant to disease progression and treatment.

Original languageEnglish (US)
Pages (from-to)850-859
Number of pages10
JournalGenome Research
Volume22
Issue number5
DOIs
StatePublished - May 1 2012
Externally publishedYes

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Microbiota
Atopic Dermatitis
Skin
Therapeutics
Disease Progression
Staphylococcus aureus
16S Ribosomal RNA
Propionibacterium
Bacteria
Bacterial Genes
Corynebacterium
Streptococcus
Staphylococcus
rRNA Genes
Skin Diseases

ASJC Scopus subject areas

  • Genetics
  • Genetics(clinical)

Cite this

Kong, H. H., Oh, J., Deming, C., Conlan, S., Grice, E. A., Beatson, M. A., ... Segre, J. A. (2012). Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Research, 22(5), 850-859. https://doi.org/10.1101/gr.131029.111

Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. / Kong, Heidi H.; Oh, Julia; Deming, Clay; Conlan, Sean; Grice, Elizabeth A.; Beatson, Melony A.; Nomicos, Effie; Polley, Eric; Komarow, Hirsh D.; Mullikin, Jim; Thomas, Jim; Blakesley, Robert; Young, Alice; Chu, Grace; Ramsahoye, Colleen; Lovett, Sean; Han, Joel; Legaspi, Richelle; Sison, Christina; Montemayor, Casandra; Gregory, Michael; Hargrove, April; Johnson, Taccara; Riebow, Nancy; Schmidt, Brian; Novotny, Betsy; Gupta, Jyoti; Benjamin, Betty; Brooks, Shelise; Coleman, Holly; Ho, Shi Ling; Schandler, Karen; Stantripop, Mal; Maduro, Quino; Bouffard, Gerry; Dekhtyar, Mila; Guan, Xiaobin; Masiello, Cathy; Maskeri, Baishali; McDowell, Jenny; Park, Morgan; Vemulapalli, Meg; Murray, Patrick R.; Turner, Maria L.; Segre, Julia A.

In: Genome Research, Vol. 22, No. 5, 01.05.2012, p. 850-859.

Research output: Contribution to journalArticle

Kong, HH, Oh, J, Deming, C, Conlan, S, Grice, EA, Beatson, MA, Nomicos, E, Polley, E, Komarow, HD, Mullikin, J, Thomas, J, Blakesley, R, Young, A, Chu, G, Ramsahoye, C, Lovett, S, Han, J, Legaspi, R, Sison, C, Montemayor, C, Gregory, M, Hargrove, A, Johnson, T, Riebow, N, Schmidt, B, Novotny, B, Gupta, J, Benjamin, B, Brooks, S, Coleman, H, Ho, SL, Schandler, K, Stantripop, M, Maduro, Q, Bouffard, G, Dekhtyar, M, Guan, X, Masiello, C, Maskeri, B, McDowell, J, Park, M, Vemulapalli, M, Murray, PR, Turner, ML & Segre, JA 2012, 'Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis', Genome Research, vol. 22, no. 5, pp. 850-859. https://doi.org/10.1101/gr.131029.111
Kong, Heidi H. ; Oh, Julia ; Deming, Clay ; Conlan, Sean ; Grice, Elizabeth A. ; Beatson, Melony A. ; Nomicos, Effie ; Polley, Eric ; Komarow, Hirsh D. ; Mullikin, Jim ; Thomas, Jim ; Blakesley, Robert ; Young, Alice ; Chu, Grace ; Ramsahoye, Colleen ; Lovett, Sean ; Han, Joel ; Legaspi, Richelle ; Sison, Christina ; Montemayor, Casandra ; Gregory, Michael ; Hargrove, April ; Johnson, Taccara ; Riebow, Nancy ; Schmidt, Brian ; Novotny, Betsy ; Gupta, Jyoti ; Benjamin, Betty ; Brooks, Shelise ; Coleman, Holly ; Ho, Shi Ling ; Schandler, Karen ; Stantripop, Mal ; Maduro, Quino ; Bouffard, Gerry ; Dekhtyar, Mila ; Guan, Xiaobin ; Masiello, Cathy ; Maskeri, Baishali ; McDowell, Jenny ; Park, Morgan ; Vemulapalli, Meg ; Murray, Patrick R. ; Turner, Maria L. ; Segre, Julia A. / Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. In: Genome Research. 2012 ; Vol. 22, No. 5. pp. 850-859.
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abstract = "Atopic dermatitis (AD) has long been associated with Staphylococcus aureus skin colonization or infection and is typically managed with regimens that include antimicrobial therapies. However, the role of microbial communities in the pathogenesis of AD is incompletely characterized. To assess the relationship between skin microbiota and disease progression, 16S ribosomal RNA bacterial gene sequencing was performed on DNA obtained directly from serial skin sampling of children with AD. The composition of bacterial communities was analyzed during AD disease states to identify characteristics associated with AD flares and improvement post-treatment. We found that microbial community structures at sites of disease predilection were dramatically different in AD patients compared with controls. Microbial diversity during AD flares was dependent on the presence or absence of recent AD treatments, with even intermittent treatment linked to greater bacterial diversity than no recent treatment. Treatment-associated changes in skin bacterial diversity suggest that AD treatments diversify skin bacteria preceding improvements in disease activity. In AD, the proportion of Staphylococcus sequences, particularly S. aureus, was greater during disease flares than at baseline or post-treatment, and correlated with worsened disease severity. Representation of the skin commensal S. epidermidis also significantly increased during flares. Increases in Streptococcus, Propionibacterium, and Corynebacterium species were observed following therapy. These findings reveal linkages between microbial communities and inflammatory diseases such as AD, and demonstrate that as compared with culture-based studies, higher resolution examination of microbiota associated with human disease provides novel insights into global shifts of bacteria relevant to disease progression and treatment.",
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AU - Beatson, Melony A.

AU - Nomicos, Effie

AU - Polley, Eric

AU - Komarow, Hirsh D.

AU - Mullikin, Jim

AU - Thomas, Jim

AU - Blakesley, Robert

AU - Young, Alice

AU - Chu, Grace

AU - Ramsahoye, Colleen

AU - Lovett, Sean

AU - Han, Joel

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AU - Sison, Christina

AU - Montemayor, Casandra

AU - Gregory, Michael

AU - Hargrove, April

AU - Johnson, Taccara

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AU - Schmidt, Brian

AU - Novotny, Betsy

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AU - Benjamin, Betty

AU - Brooks, Shelise

AU - Coleman, Holly

AU - Ho, Shi Ling

AU - Schandler, Karen

AU - Stantripop, Mal

AU - Maduro, Quino

AU - Bouffard, Gerry

AU - Dekhtyar, Mila

AU - Guan, Xiaobin

AU - Masiello, Cathy

AU - Maskeri, Baishali

AU - McDowell, Jenny

AU - Park, Morgan

AU - Vemulapalli, Meg

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