Association of Systemic Antibiotic Treatment of Acne with Skin Microbiota Characteristics

Anna L. Chien, Jerry Tsai, Sherry Leung, Emmanuel F. Mongodin, Amanda M. Nelson, Sewon Kang, Luis A. Garza

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

Importance: Given the widespread use of systemic antibiotics for treatment of moderate to severe acne, it is important to understand the associations of such antibiotic use with changes not only in Cutibacterium acnes (formerly Propionibacterium acnes) but also in the complete bacterial community of the skin. Objective: To examine the composition, diversity, and resilience of skin microbiota associated with systemic antibiotic perturbation in individuals with acne. Design, Setting, and Participants: This longitudinal cohort study conducted at an academic referral center in Maryland from February 11 to September 23, 2014, included 4 female participants who had received a recent diagnosis of acne vulgaris, showed comedonal and inflammatory acne on the face, were at least 18 years old, and had no recent use of systemic or topical treatments for acne, including antibiotics and retinoids. Data analysis was performed between July 5, 2017, and November 7, 2018. Interventions: Participants were prescribed oral minocycline, 100 mg, twice daily for 4 weeks. Skin areas on the forehead, cheek, and chin were sampled for 16S ribosomal RNA gene sequencing at baseline, 4 weeks after starting minocycline treatment, and then 1 week and 8 weeks after discontinuation of treatment. Main Outcomes and Measures: Skin microbiota examined with respect to relative abundance of bacterial taxa, α diversity (represents within-sample microbial diversity), and β diversity (represents between-sample microbial diversity). Acne status evaluated with photography and lesion count. Results: Of the 4 patients included in this study, 2 were 25 years old, 1 was 29 years old, and 1 was 35 years old; 2 were white women, 1 was an African American woman, and 1 was an Asian woman. Across all 4 patients, antibiotic treatment was associated with a 1.4-fold reduction in the level of C acnes (difference, -10.3%; 95% CI, -19.9% to -0.7%; P =.04) with recovery following cessation of treatment. Distinct patterns of change were identified in multiple bacterial genera, including a transient 5.6-fold increase in the relative abundance of Pseudomonas species (difference, 2.2%; 95% CI, 0.9%-3.4%; P <.001) immediately following antibiotic treatment, as well as a persistent 1.7-fold increase in the relative abundance of Streptococcus species (difference, 5.4%; 95% CI, 0.3%-10.6%; P =.04) and a 4.7-fold decrease in the relative abundance of Lactobacillus species (difference, -0.8%; 95% CI, -1.4% to -0.2%; P =.02) 8 weeks following antibiotic treatment withdrawal. In general, antibiotic administration was associated with an initial decrease from baseline of bacterial diversity followed by recovery. Principal coordinates analysis results showed moderate clustering of samples by patient (analysis of similarity, R = 0.424; P =.001) and significant clustering of samples by time in one participant (analysis of similarity, R = 0.733; P =.001). Conclusions and Relevance: In this study, systemic antibiotic treatment of acne was associated with changes in the composition and diversity of skin microbiota, with variable rates of recovery across individual patients and parallel changes in specific bacterial populations. Understanding the association between systemic antibiotic use and skin microbiota may help clinicians decrease the likelihood of skin comorbidities related to microbial dysbiosis.

Original languageEnglish (US)
Pages (from-to)425-434
Number of pages10
JournalJAMA Dermatology
Volume155
Issue number4
DOIs
StatePublished - Apr 2019

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Microbiota
Acne Vulgaris
Anti-Bacterial Agents
Skin
Minocycline
Therapeutics
Cluster Analysis
Dysbiosis
16S Ribosomal RNA
RNA Sequence Analysis
Propionibacterium acnes
Chin
Withholding Treatment
Forehead
Cheek
Photography
Retinoids
Lactobacillus
Pseudomonas
Streptococcus

All Science Journal Classification (ASJC) codes

  • Dermatology

Cite this

Chien, Anna L. ; Tsai, Jerry ; Leung, Sherry ; Mongodin, Emmanuel F. ; Nelson, Amanda M. ; Kang, Sewon ; Garza, Luis A. / Association of Systemic Antibiotic Treatment of Acne with Skin Microbiota Characteristics. In: JAMA Dermatology. 2019 ; Vol. 155, No. 4. pp. 425-434.
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title = "Association of Systemic Antibiotic Treatment of Acne with Skin Microbiota Characteristics",
abstract = "Importance: Given the widespread use of systemic antibiotics for treatment of moderate to severe acne, it is important to understand the associations of such antibiotic use with changes not only in Cutibacterium acnes (formerly Propionibacterium acnes) but also in the complete bacterial community of the skin. Objective: To examine the composition, diversity, and resilience of skin microbiota associated with systemic antibiotic perturbation in individuals with acne. Design, Setting, and Participants: This longitudinal cohort study conducted at an academic referral center in Maryland from February 11 to September 23, 2014, included 4 female participants who had received a recent diagnosis of acne vulgaris, showed comedonal and inflammatory acne on the face, were at least 18 years old, and had no recent use of systemic or topical treatments for acne, including antibiotics and retinoids. Data analysis was performed between July 5, 2017, and November 7, 2018. Interventions: Participants were prescribed oral minocycline, 100 mg, twice daily for 4 weeks. Skin areas on the forehead, cheek, and chin were sampled for 16S ribosomal RNA gene sequencing at baseline, 4 weeks after starting minocycline treatment, and then 1 week and 8 weeks after discontinuation of treatment. Main Outcomes and Measures: Skin microbiota examined with respect to relative abundance of bacterial taxa, α diversity (represents within-sample microbial diversity), and β diversity (represents between-sample microbial diversity). Acne status evaluated with photography and lesion count. Results: Of the 4 patients included in this study, 2 were 25 years old, 1 was 29 years old, and 1 was 35 years old; 2 were white women, 1 was an African American woman, and 1 was an Asian woman. Across all 4 patients, antibiotic treatment was associated with a 1.4-fold reduction in the level of C acnes (difference, -10.3{\%}; 95{\%} CI, -19.9{\%} to -0.7{\%}; P =.04) with recovery following cessation of treatment. Distinct patterns of change were identified in multiple bacterial genera, including a transient 5.6-fold increase in the relative abundance of Pseudomonas species (difference, 2.2{\%}; 95{\%} CI, 0.9{\%}-3.4{\%}; P <.001) immediately following antibiotic treatment, as well as a persistent 1.7-fold increase in the relative abundance of Streptococcus species (difference, 5.4{\%}; 95{\%} CI, 0.3{\%}-10.6{\%}; P =.04) and a 4.7-fold decrease in the relative abundance of Lactobacillus species (difference, -0.8{\%}; 95{\%} CI, -1.4{\%} to -0.2{\%}; P =.02) 8 weeks following antibiotic treatment withdrawal. In general, antibiotic administration was associated with an initial decrease from baseline of bacterial diversity followed by recovery. Principal coordinates analysis results showed moderate clustering of samples by patient (analysis of similarity, R = 0.424; P =.001) and significant clustering of samples by time in one participant (analysis of similarity, R = 0.733; P =.001). Conclusions and Relevance: In this study, systemic antibiotic treatment of acne was associated with changes in the composition and diversity of skin microbiota, with variable rates of recovery across individual patients and parallel changes in specific bacterial populations. Understanding the association between systemic antibiotic use and skin microbiota may help clinicians decrease the likelihood of skin comorbidities related to microbial dysbiosis.",
author = "Chien, {Anna L.} and Jerry Tsai and Sherry Leung and Mongodin, {Emmanuel F.} and Nelson, {Amanda M.} and Sewon Kang and Garza, {Luis A.}",
year = "2019",
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doi = "10.1001/jamadermatol.2018.5221",
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Association of Systemic Antibiotic Treatment of Acne with Skin Microbiota Characteristics. / Chien, Anna L.; Tsai, Jerry; Leung, Sherry; Mongodin, Emmanuel F.; Nelson, Amanda M.; Kang, Sewon; Garza, Luis A.

In: JAMA Dermatology, Vol. 155, No. 4, 04.2019, p. 425-434.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Association of Systemic Antibiotic Treatment of Acne with Skin Microbiota Characteristics

AU - Chien, Anna L.

AU - Tsai, Jerry

AU - Leung, Sherry

AU - Mongodin, Emmanuel F.

AU - Nelson, Amanda M.

AU - Kang, Sewon

AU - Garza, Luis A.

PY - 2019/4

Y1 - 2019/4

N2 - Importance: Given the widespread use of systemic antibiotics for treatment of moderate to severe acne, it is important to understand the associations of such antibiotic use with changes not only in Cutibacterium acnes (formerly Propionibacterium acnes) but also in the complete bacterial community of the skin. Objective: To examine the composition, diversity, and resilience of skin microbiota associated with systemic antibiotic perturbation in individuals with acne. Design, Setting, and Participants: This longitudinal cohort study conducted at an academic referral center in Maryland from February 11 to September 23, 2014, included 4 female participants who had received a recent diagnosis of acne vulgaris, showed comedonal and inflammatory acne on the face, were at least 18 years old, and had no recent use of systemic or topical treatments for acne, including antibiotics and retinoids. Data analysis was performed between July 5, 2017, and November 7, 2018. Interventions: Participants were prescribed oral minocycline, 100 mg, twice daily for 4 weeks. Skin areas on the forehead, cheek, and chin were sampled for 16S ribosomal RNA gene sequencing at baseline, 4 weeks after starting minocycline treatment, and then 1 week and 8 weeks after discontinuation of treatment. Main Outcomes and Measures: Skin microbiota examined with respect to relative abundance of bacterial taxa, α diversity (represents within-sample microbial diversity), and β diversity (represents between-sample microbial diversity). Acne status evaluated with photography and lesion count. Results: Of the 4 patients included in this study, 2 were 25 years old, 1 was 29 years old, and 1 was 35 years old; 2 were white women, 1 was an African American woman, and 1 was an Asian woman. Across all 4 patients, antibiotic treatment was associated with a 1.4-fold reduction in the level of C acnes (difference, -10.3%; 95% CI, -19.9% to -0.7%; P =.04) with recovery following cessation of treatment. Distinct patterns of change were identified in multiple bacterial genera, including a transient 5.6-fold increase in the relative abundance of Pseudomonas species (difference, 2.2%; 95% CI, 0.9%-3.4%; P <.001) immediately following antibiotic treatment, as well as a persistent 1.7-fold increase in the relative abundance of Streptococcus species (difference, 5.4%; 95% CI, 0.3%-10.6%; P =.04) and a 4.7-fold decrease in the relative abundance of Lactobacillus species (difference, -0.8%; 95% CI, -1.4% to -0.2%; P =.02) 8 weeks following antibiotic treatment withdrawal. In general, antibiotic administration was associated with an initial decrease from baseline of bacterial diversity followed by recovery. Principal coordinates analysis results showed moderate clustering of samples by patient (analysis of similarity, R = 0.424; P =.001) and significant clustering of samples by time in one participant (analysis of similarity, R = 0.733; P =.001). Conclusions and Relevance: In this study, systemic antibiotic treatment of acne was associated with changes in the composition and diversity of skin microbiota, with variable rates of recovery across individual patients and parallel changes in specific bacterial populations. Understanding the association between systemic antibiotic use and skin microbiota may help clinicians decrease the likelihood of skin comorbidities related to microbial dysbiosis.

AB - Importance: Given the widespread use of systemic antibiotics for treatment of moderate to severe acne, it is important to understand the associations of such antibiotic use with changes not only in Cutibacterium acnes (formerly Propionibacterium acnes) but also in the complete bacterial community of the skin. Objective: To examine the composition, diversity, and resilience of skin microbiota associated with systemic antibiotic perturbation in individuals with acne. Design, Setting, and Participants: This longitudinal cohort study conducted at an academic referral center in Maryland from February 11 to September 23, 2014, included 4 female participants who had received a recent diagnosis of acne vulgaris, showed comedonal and inflammatory acne on the face, were at least 18 years old, and had no recent use of systemic or topical treatments for acne, including antibiotics and retinoids. Data analysis was performed between July 5, 2017, and November 7, 2018. Interventions: Participants were prescribed oral minocycline, 100 mg, twice daily for 4 weeks. Skin areas on the forehead, cheek, and chin were sampled for 16S ribosomal RNA gene sequencing at baseline, 4 weeks after starting minocycline treatment, and then 1 week and 8 weeks after discontinuation of treatment. Main Outcomes and Measures: Skin microbiota examined with respect to relative abundance of bacterial taxa, α diversity (represents within-sample microbial diversity), and β diversity (represents between-sample microbial diversity). Acne status evaluated with photography and lesion count. Results: Of the 4 patients included in this study, 2 were 25 years old, 1 was 29 years old, and 1 was 35 years old; 2 were white women, 1 was an African American woman, and 1 was an Asian woman. Across all 4 patients, antibiotic treatment was associated with a 1.4-fold reduction in the level of C acnes (difference, -10.3%; 95% CI, -19.9% to -0.7%; P =.04) with recovery following cessation of treatment. Distinct patterns of change were identified in multiple bacterial genera, including a transient 5.6-fold increase in the relative abundance of Pseudomonas species (difference, 2.2%; 95% CI, 0.9%-3.4%; P <.001) immediately following antibiotic treatment, as well as a persistent 1.7-fold increase in the relative abundance of Streptococcus species (difference, 5.4%; 95% CI, 0.3%-10.6%; P =.04) and a 4.7-fold decrease in the relative abundance of Lactobacillus species (difference, -0.8%; 95% CI, -1.4% to -0.2%; P =.02) 8 weeks following antibiotic treatment withdrawal. In general, antibiotic administration was associated with an initial decrease from baseline of bacterial diversity followed by recovery. Principal coordinates analysis results showed moderate clustering of samples by patient (analysis of similarity, R = 0.424; P =.001) and significant clustering of samples by time in one participant (analysis of similarity, R = 0.733; P =.001). Conclusions and Relevance: In this study, systemic antibiotic treatment of acne was associated with changes in the composition and diversity of skin microbiota, with variable rates of recovery across individual patients and parallel changes in specific bacterial populations. Understanding the association between systemic antibiotic use and skin microbiota may help clinicians decrease the likelihood of skin comorbidities related to microbial dysbiosis.

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