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    Allergy Asthma Immunol Res. 2023 Sep;15(5):659-672. English.
    Published online Jul 06, 2023.
    https://doi.org/10.4168/aair.2023.15.5.659
    Copyright © 2023 The Korean Academy of Asthma, Allergy and Clinical Immunology • The Korean Academy of Pediatric Allergy and Respiratory Disease
    Original Article

    Association Between Nasal Colonization of Staphylococcus aureus and Eczema of Multiple Body Sites

    Yang Guo,1 Xia Dou,1 Xiao-Fan Chen,2 Cong Huang,1 Ying-Jie Zheng,3,4 and Bo Yu1
      • 1Department of Dermatology, Institute of Dermatology, Peking University Shenzhen Hospital, Shenzhen Peking University - The Hong Kong University of Science and Technology Medical Center, Shenzhen, China.
      • 2Biomedical Research Institute, Shenzhen Peking University - The Hong Kong University of Science and Technology Medical Center, Shenzhen, China.
      • 3Department of Epidemiology, School of Public Health, Fudan University, Shanghai, China.
      • 4Key Laboratory for Health Technology Assessment, National Commission of Health and Family Planning, Shanghai, China.
    • Correspondence to Bo Yu, MD. Department of Dermatology, Institute of Dermatology, Peking University Shenzhen Hospital, Shenzhen Peking University - The Hong Kong University of Science and Technology Medical Center, No. 1120, Lianhua Rd, Shenzhen, Guangdong 518036, China. Tel: +86-0755-83910721; Fax: +86-0755-83910721; Email: drboyu_derm@126.com
      Correspondence to Ying-Jie Zheng, PhD. Department of Epidemiology, School of Public Health, Fudan University and Key Laboratory for Health Technology Assessment, National Commission of Health and Family Planning, No. 130 Dong’an Rd, Xuhui District, Shanghai 200032, China. Tel: +86-13764425579; Email: yjzheng@fudan.edu.cn
    Received February 11, 2023; Revised April 17, 2023; Accepted April 20, 2023.

    This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

    Abstract

    Purpose

    Staphylococcus aureus is the critical pathogenic bacterium of eczema. The relationship between nasal colonization by S. aureus and eczema has not been well studied. We aimed to evaluate the associations between nasal colonization by S. aureus and eczema of multiple body sites, including persistent and ever-reported eczema. We further examined the associations between eczema and different subtypes of S. aureus, that is, methicillin-resistant S. aureus (MRSA) and methicillin-sensitive S. aureus (MSSA).

    Methods

    The real-world data from the US National Health and Nutrition Examination Survey were used. The associations were calculated using survey-weighted multinomial logistic regression models and further calculated in subgroups stratified by demographic factors.

    Results

    In total, 2,941 adults were included. The prevalence rate of S. aureus nasal carriage was significantly higher in adults with persistent hand eczema (51.0%) than in those with ever-reported hand eczema (23.3%) and never eczema (26.9%). S. aureus nasal colonization was associated with an approximately two-fold increased risk of persistent hand eczema (odds ratios ranges in different models: 2.86–3.06) without significant heterogeneity in the association by demographic factors. No significant associations between S. aureus nasal colonization and persistent eczema of other body sites or ever-reported eczema of multiple body sites (including hands) were observed. Furthermore, similar significant association between nasal colonization of MSSA and persistent hand eczema was seen; the association was much stronger (odds ratios ranges in different models: 4.64–6.54) for MRSA, although with borderline significant.

    Conclusions

    Nasal colonization of S. aureus was associated with increased risk of persistent hand eczema. Our findings imply that preventive measures targeting S. aureus for the anterior nares should be considered in preventing and treating eczema.

    Keywords
    Epidemiology; atopic dermatitis; Staphylococcus aureus; NHANES

    INTRODUCTION

    Eczema, also known as atopic dermatitis and atopic eczema, is one of the most common inflammatory skin disorders, with prevalence rates of 20% in children and 10% in adults.1, 2 The pathogenesis of eczema is complex and multifactorial.3, 4 Staphylococcus aureus is the critical pathogenic bacterium in the pathogenesis of eczema and can lead to dysbiosis of the skin microbiome.5, 6, 7 S. aureus contributes to eczema pathogenesis in multiple ways, including production of various virulence factors associated with eczema-related proinflammatory responses, epidermal barrier dysfunction, and expression of proteins that protect S. aureus from antimicrobial peptides, etc.6, 8, 9

    Previous studies have focused mainly on the role of skin colonization of S. aureus on eczema. The abundance of S. aureus on the skin is correlated with the increased severity of eczema.10, 11 However, the relationship between nasal colonization by S. aureus and eczema has not been clearly investigated. Regarding the source and spread of S. aureus colonized on the skin, the nasal and nasopharyngeal areas may function as important reservoirs for S. aureus to spread from the nose to multiple body sites,12 such as the hands and arms. According to a study of infants, nasal colonization of S. aureus at the age of 6 months and frequent colonization in the first year of life were associated with eczema and its severity.13 However, inconsistent findings have been reported.14, 15

    Antimicrobial resistance is a major concern about eczema and specific emphasis on this issue is often placed on methicillin-resistant S. aureus (MRSA).16 Several small-scale studies have reported that the prevalence rates of nasal colonization of MRSA among eczema cases varied from 0% to 22.5%.17, 18, 19 However, studies on the specific contribution of nasal colonization of MRSA to eczema are limited.

    Therefore, in the present study, we aimed to examine the associations between nasal colonization by S. aureus and eczema of multiple body sites, including persistent and ever-reported eczema. We also aimed to further evaluate the associations between eczema and different subtypes of S. aureus, that is, MRSA and methicillin-sensitive S. aureus (MSSA).

    MATERIALS AND METHODS

    Study population

    We used anonymous publicly available data from the US National Health and Nutrition Examination Survey (NHANES), which is a series of national population-based surveys conducted by the National Center for Health Statistics (NCHS). A stratified, randomized, multistage, probability-cluster design was employed to select participants in the NHANES; thus, the participants for the NHANES could represent the national population of US.20 The NHANES were approved by the NCHS institutional review board, and informed consent was obtained from all participants.21 For the present study, all the available data of NHANES 2003–2004 participants with information on S. aureus nasal colonization and eczema were included. A total of 10,122 participants were interviewed, among which 6,987 participants with missing information on eczema and 194 participants with missing information on S. aureus nasal colonization were excluded. Finally, a total of 2,941 participants, including persistent eczema (n = 200), ever-reported eczema (n = 161), and never eczema (n = 2,580), were included for the present analyses. The flowchart and participants’ eligibility criteria are shown in the Supplementary Fig. S1.

    Assessment of eczema

    We obtained the information on eczema from the Questionnaire Data section of the NHANES.22 The information on eczema was collected through personal interviews by professional staff among participants aged 20–59 years. For our current analyses, variables related to eczema were new ones generated based on responses to the following questions in the Questionnaire Data section. The ever-reported eczema was assessed by the question “During the past 12 months, have you had dermatitis, eczema, or any other type of red, inflamed skin rash?” (Yes) and the question “Do you have this skin condition today?” (No) (Supplementary Table S1). Accordingly, persistent eczema was defined as an affirmative response to the above 2 questions. Furthermore, for participants with eczema, the body sites of eczema were assessed through the questions “Hands affected by skin conditions?,” “Arms affected by skin conditions?,” etc. (Supplementary Table S1).

    Assessment of S. aureus nasal colonization

    Nasal swab samples were collected from both anterior nares using a culture swab and plated on mannitol salt agar (MSA), a selective medium for the isolation of S. aureus. A rapid latex kit (Staphaurex; Thermo Fisher Scientific, Waltham, MA, USA) and a tube coagulase test were used to identify S. aureus. S. aureus isolates were further screened for methicillin resistance and the National Committee for Clinical Laboratory Standards disk diffusion method was used to identify MRSA and MSSA. Further details have previously been described.22

    For our study, S. aureus nasal colonization was assessed using the variable “S. aureus present” in the Laboratory Data section (Supplementary Table S1). For participants with S. aureus nasal colonization, MRSA was defined as an affirmative response to variable “MRSA (methicillin-resistant S. aureus).” Otherwise, participants with S. aureus nasal colonization without MRSA were regarded as MSSA colonization.22

    Assessment of covariates

    Demographic variables, including age, sex, race, education level, and family poverty income ratio (PIR), were obtained from the Demographics Data section (Supplementary Table S1). Race groups were categorized into “non-Hispanic White,” “non-Hispanic Black,” “Mexican American,” and “others.” Education levels were categorized as “high school or lower,” “some college,” and “college degree or higher” according to responses to “What is the highest grade or level of school completed or the highest degree received?” As a marker of socioeconomic status, the family PIR is the ratio of family income to poverty threshold and was categorized into < 4 and ≥ 4.

    Lifestyle factors, including smoking, alcohol consumption, and body mass index (BMI), were also considered. Smoking was based on responses to “Do you now smoke cigarettes?” in the Questionnaire Data section, and this variable was classified as “not at all,” “some days,” and “every day” (Supplementary Table S1). Alcohol drinking was dichotomized into ≤ 12 or > 12 based on responses to “Had at least 12 alcohol drinks/year?”. BMI information was obtained from the Examination Data section and was classified into 3 groups: normal weight/underweight (BMI < 25 kg/m2), overweight (25 kg/m2 ≤ BMI < 30 kg/m2), and obesity (BMI ≥ 30 kg/m2).

    Furthermore, S. aureus nasal carriage is associated with asthma23, 24 and asthma was also considered in our study. In detail, asthma was defined as an affirmative response to the question “Has a doctor or other health professional ever told you that you have asthma?” (Supplementary Table S1). In addition, as healthcare utilization may also increase the risk of S. aureus colonization, we include the variable of healthcare utilization in our analyses, which was assessed through the questions “During the past 12 months, how many times have you seen a doctor or other health care professional about your health at a doctor’s office, a clinic, hospital emergency department, at home, or some other place?” (Supplementary Table S1).

    Statistical analysis

    Statistical analyses were conducted using SAS software (version 9.4; SAS Institute, Cary, NC, USA). For NHANES data, the survey results were weighted to represent the US national population, accounting for the complex survey design, survey nonresponse, and poststratification.20 Therefore, we used NHANES cluster design variables (SDMVSTRA and SDMVPSU) and the weight variable (WTMEC2YR); accordingly, SAS SURVEY procedures were used.

    We compared the characteristics of the study population by weight change patterns using the Rao-Scott χ2 test for categorical variables and analysis of variance adjusted for sampling weights for continuous variables.25 To estimate the odds ratios (ORs) and 95% confidence intervals (CIs) of eczema according to S. aureus nasal colonization, we constructed survey-weighted multinomial logistic regression models with eczema as the dependent variable (“persistent eczema” and “ever-reported eczema” to a reference level of “never eczema”) and S. aureus nasal colonization as the independent variable.26 Three models were provided: model 1 (the crude model), model 2 (adjustment for age, sex, and race), and model 3 (adjustment for age, sex, race, education, family PIR, asthma, and healthcare utilization). In addition, to determine whether the associations varied by participant characteristics, we examined the associations in subgroups stratified by demographic factors, including age, sex, race, education level, and family PIR. P values for heterogeneity were calculated to evaluate the heterogeneity of the ORs across stratums.27 Furthermore, to evaluate the specific associations between eczema and different subtypes of S. aureus, including MRSA and MSSA, we calculated ORs and 95% CIs of eczema according to MRSA (MRSA vs. no S. aureus) and MSSA (MSSA vs. no S. aureus), respectively. All P values were two-tailed, and a P value of < 0.05 was considered statistically significant.

    RESULTS

    Characteristics of the study population

    We included 2,941 participants in the current analyses (Table 1), including persistent eczema (n = 200), ever-reported eczema (n = 161), and never eczema (n = 2,580). As eczema information was only available in individuals aged 20–59 years, the major characteristics between those included and the individuals aged 20–59 excluded were compared; no significant differences in characteristics other than race and asthma between the 2 groups were seen (Supplementary Table S2). The enrolled participants with eczema tended to be older, more likely to be non-Hispanic White, and had a higher level of education, family PIR, and healthcare utilization (Table 1). Furthermore, characteristics other than race and BMI were similar in the carriage of S. aureus (Supplementary Table S3) and subtype of S. aureus (Supplementary Table S4).

    Table 1
    Characteristics of study population according to the status of eczema

    The prevalence rates of nasal colonization of S. aureus for eczema of multiple body sites

    The results are shown in Table 2. The prevalence rate of S. aureus was significantly higher in persistent hand eczema (51.0%) than in ever-reported hand eczema (23.3%) and in never eczema (26.9%) (P = 0.006). No significant differences of prevalence between the 3 groups (persistent eczema, ever-reported eczema, and never eczema) were observed in other body sites, including the arm, head/face/neck, shoulder, and torso (all P > 0.05).

    Table 2
    Nasal colonization of S. aureus in multiple body sites according to the status of eczema

    Associations between S. aureus nasal colonization and persistent eczema of multiple body sites

    As shown in Table 3, model 1 showed that S. aureus nasal colonization was associated with an increased risk of persistent hand eczema (model 1: OR, 2.86; 95% CI, 1.54–5.31; P < 0.001). Significant associations were also observed in model 2 (OR, 3.06; 95% CI, 1.61–5.81; P < 0.001) and model 3 (OR, 2.99; 95% CI, 1.64–5.46; P < 0.001). In contrast, we did not find any significant associations between S. aureus nasal colonization and persistent eczema of other body sites, including arm, head/face/neck, shoulder, or torso.

    Table 3
    ORs and 95% CIs for persistent eczema of multiple body sites according to S. aureus and subtypes of S. aureus nasal colonization

    We further evaluated whether the associations between S. aureus nasal colonization and persistent hand eczema varied according to participant characteristics. No statistically significant evidence of heterogeneity was found in the association among participants with different demographic factors (Figure A).

    Figure
    Associations between S. aureus and MSSA nasal colonization and persistent hand eczema stratified by demographic factors.
    (A) Associations between S. aureus nasal colonization and persistent hand eczema stratified by demographic factors. (B) Associations between MSSA nasal colonization and persistent hand eczema stratified by demographic factors.

    MSSA, methicillin-sensitive S. aureus; MRSA, methicillin-resistant S. aureus; PIR, poverty income ratio; OR, odds ratio; CI, confidence interval.

    *Survey-weighted multinomial logistic regression adjusted for age, sex, race, education, family PIR, asthma, and healthcare utilization; †Levels correspond to the median distribution of age.

    Associations between nasal colonization of MRSA and MSSA and persistent eczema of multiple body sites

    We found that nasal colonization of MSSA was significantly associated with persistent hand eczema based on model 1 (OR, 2.78; 95% CI, 1.30–5.94; P = 0.008), model 2 (OR, 2.98; 95% CI, 1.36–6.53; P = 0.007), and model 3 (OR, 2.87; 95% CI, 1.37–6.02; P = 0.005) (Table 3). For MRSA, the trend for an increased risk of persistent hand eczema was seen, but the sample size of MRSA cases was limited; the ORs in models 1, 2, and 3 were 4.64 (95% CI, 0.91–23.78; P = 0.066), 4.84 (95% CI, 0.93–25.15; P = 0.061), and 6.54 (95% CI, 1.44–29.70; P = 0.015), respectively. No significant associations were observed between MSSA nasal colonization and persistent eczema of the arm, head/face/neck, shoulder, and torso. Similarly, for MRSA, no significant associations were observed for the arm or the shoulder.

    We further conducted stratified analyses by demographic factors for the association between nasal colonization of MSSA and persistent hand eczema. We did not find significant heterogeneity in the associations with age, sex, race, or family PIR. The test for heterogeneity was marginally significant for the education level (Figure B).

    Associations between S. aureus nasal colonization and ever-reported eczema of multiple body sites

    No significant associations between S. aureus nasal colonization and ever-reported hand eczema were found in models 1, 2, or 3 (Table 4). Similarly, for other body sites, including the arm, head/face/neck, shoulder, and torso, we did not find any significant associations between S. aureus nasal colonization and ever-reported eczema of these body sites.

    Table 4
    ORs and 95% CIs for ever-reported eczema of multiple body sites according to S. aureus and subtypes of S. aureus nasal colonization

    Associations between nasal colonization of MRSA and MSSA and ever-reported eczema of multiple body sites

    Regarding ever-reported eczema, we also analyzed specific associations between ever-reported eczema and different subtypes of S. aureus. We did not find significant associations between MSSA colonization and ever-reported eczema of all above-mentioned body sites (Table 4). For MRSA, no significant association was observed for ever-reported eczema of the arm.

    DISCUSSION

    Our results showed that nasal colonization of S. aureus was associated with increased risk of persistent eczema of the hand, but not of the other body sites or for ever-reported eczema. The association between nasal colonization of MRSA and persistent hand eczema was stronger, although borderline significant. Our findings offer new insights into the prevention of eczema, indicating that preventive measures for the anterior nares could be considered.

    For the observed phenomenon, our hypothesis is that the nose acts as an important middle reservoir of S. aureus, which may transmit from the hands to the nose and recolonize back to hands; this is called “hands-nose-hands cycle” (Supplementary Fig. S2). Specifically, the hand plays an important role in infections, either nosocomial or non-nosocomial. Patients with hand eczema have intense itching, and the frequency of scratching and touching increases. As a result, the mutual contact between hands and other body sites often causes self-inoculation of pathogens, especially those from hands.12 Thus, hand washing is considered a highly cost-effective measure for the prevention of pathogen transmission. Without effective hand washing, pathogens colonized on hands may spread back to the nose through the fingers, forming hands-nose-hands transmission cycles. Furthermore, colonization of drug-resistant bacteria, which leads to persistent and chronic infection, may enhance the cycles above.28 As reported, the frequency of hand-to-nose touching was similar to that of hand-to-chin touching with the highest frequency among the hand-to-T-zone touching studies.29 Touching occurs more frequently in the face than in other body parts.30 Furthermore, nasal colonization of S. aureus is associated with allergic rhinitis,31 chronic rhinosinusitis,32 and chronic rhinosinusitis with nasal polyps (CRSwNP).33 The virulence factors and enterotoxins from S. aureus could promote inflammation of nasal mucosa34 and play a critical role in the pathogenesis of these upper airway diseases. These upper airway diseases may also be involved in the relationship between nasal colonization of S. aureus and hand eczema.

    Previous studies have also implied that the anterior nares was an important harbor for S. aureus. 13, 35, 36 For S. aureus transmission, 2 studies conducted in children12, 37 showed that S. aureus might transmit from the nose to the skin through their own fingers, which is consistent with our hypothesis of the hands-nose-hands cycles. Additionally, the same S. aureus strains were found in the nose and skin of patients,38 and microbiome studies found species correlations in the nose and on the skin, indicating probable cross-transmission of bacteria between these niches.39, 40, 41 Of note, most of the participants in these studies were children. Our adult study observed similar phenomena, which were stable within different demographic strata. Moreover, regarding the potential mechanisms of S. aureus spread and recolonization, biofilm production by S. aureus strains colonizing the anterior nares is crucial for dispersal and persistent colonization of the skin.42

    In line with our findings, a significant association between nasal colonization of S. aureus and eczema has been reported in other cross-sectional35 and cohort studies.13, 14 Additionally, detailed analyses suggested that the presence of S. aureus nasal colonization is related to increased disease severity in eczema.35, 43, 44 However, controversial results have also been reported.14, 15 For instance, Hu et al. revealed that there was the cross-sectional, but not longitudinal, association between S. aureus nasal carriage and eczema.14 The difference between conflicting results might be explained by differences in the study population (adults vs. children), methods of sample collection, and methods of bacterial detection.

    To our knowledge, this is the first report on the relationship between S. aureus nasal colonization and persistent eczema/ever-reported eczema on the basis of a single population. In addition to persistent eczema, we did not find any association between S. aureus nasal carriage and ever-reported eczema, although previous studies44, 45 showed that S. aureus colonization on hands contributes to the chronic course of hand eczema. In contrast to persistent eczema, those with ever-reported eczema may lose persistent colonization of S. aureus on hands, which may be eradicated by treatment; as a result, the hands-nose-hands transmission of S. aureus (hands-nose-hands cycles) has been interrupted. Taken together, the nose may act as a middle reservoir of S. aureus, which may transmit from the hands to the nose and recolonize the hands through fingers (hands-nose-hands cycles). This may partially explain the phenomena observed in the present study.

    The treatment of S. aureus infection in eczema is based mainly on antibiotic therapy, and specific emphasis is placed on MRSA. This is a group of strains that are resistant to multiple β-lactam antibiotics.16 Our study found a significant association between nasal colonization of MSSA and persistent hand eczema. Larger ORs with borderline significant associations were seen for MRSA due to limited sample size. For MRSA colonization on hands, the infection appears to be more likely to persist because of antimicrobial resistance, and the hands-nose-hands cycle may be enhanced. A recent study reported a significant association between MRSA and disease severity of eczema.17 However, these results were controversial.46 Notably, previous studies have reported conflicting results, and these studies were limited by small sample sizes. A larger study is needed to address this issue.

    The strengths of our study are as follows. Our study is a national population-based one with a relatively large sample size, representing the national general adult population in the United States. To our knowledge, this is the most comprehensive report on the relationship between S. aureus nasal colonization and persistent eczema/ever-reported eczema of multiple body sites on the basis of a single population. Due to such a study design, we were able to compare the associations for persistent eczema and ever-reported eczema on the basis of a single population; the findings could help explain our opinion of “hands-nose-hands cycles” (Supplementary Fig. S2). Additionally, we reported the specific contribution of nasal colonization of both MRSA and MSSA to eczema; these related findings also supported our opinion of hands-nose-hands cycles.

    Our study had several implications. The nasal colonization of S. aureus specific to persistent eczema on hands indicates that any intervention aimed at the treatment of the nose is important for the interruption of the “hands-nose-hands cycles” for transmission of S. aureus. This will reduce the abundance of S. aureus on the skin and the transmission cycles as well as further lessen the pathogenesis of eczema. Therefore, measures focusing on the anterior nares against S. aureus infection could be considered for the prevention and adjuvant treatment of skin eczema.

    This study has several limitations. First, due to the cross-sectional design, we cannot infer a causal relationship. Secondly, self-reporting eczema and affected body sites may be subject to potential recall bias. Thirdly, detailed information on the severity of eczema or the evaluation of upper airway diseases is not available among the included participants. In addition, the number of MRSA infection was low, and the association was only borderline in significance; thus, the extrapolation and interpretation in terms of the association between MRSA infection and hand eczema should be cautious. Future studies with a larger sample size, more information evaluated, and multiple sample collections and follow-ups are needed to verify these findings.

    In conclusion, nasal colonization of S. aureus was associated with increased risk of persistent hand eczema. Our findings offer new insights into the prevention of eczema, indicating that preventive measures for the anterior nares should be considered in eczema management.

    SUPPLEMENTARY MATERIALS

    Supplementary Table S1

    Questions used in the present studies

    Click here to view.(30K, xls)

    Supplementary Table S2

    Characteristics of the included individuals and excluded individuals aged 20–59

    Click here to view.(33K, xls)

    Supplementary Table S3

    Characteristics of study population according to status of S. aureus infection

    Click here to view.(33K, xls)

    Supplementary Table S4

    Characteristics of study population according to status of subtype of the S. aureus infection

    Click here to view.(32K, xls)

    Supplementary Fig. S1

    Flowchart for the selection of study participants.

    Click here to view.(1M, ppt)

    Supplementary Fig. S2

    Illustration of the “hands-nose-hands cycle”.

    Click here to view.(822K, ppt)

    Notes

    Disclosure:There are no financial or other issues that might lead to a conflict of interest.

    ACKNOWLEDGMENTS

    This work was supported by the National Natural Science Foundation of China (No. 82103727, 81803138, and 82173582), the fellowship of China Postdoctoral Science Foundation (No. 2021M702221), Guangdong Basic and Applied Basic Research Foundation (No. 2022A1515010957 and 2021A1515011558), Shenzhen Sanming Project (No. SZSM201812059), Shenzhen Key Medical Discipline Construction Fund (No. SZXK040), Shenzhen Science and Technology Program (No. RCBS20210706092408008), and the Scientific Research Foundation of PEKING UNIVERSITY SHENZHEN HOSPITAL (No. KYQD2021039).

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    MeSH Terms
    Adult
    Colon*
    Demography
    Dermatitis, Atopic
    Eczema*
    Epidemiology
    Hand
    Humans
    Logistic Models
    Methicillin Resistance
    Methicillin-Resistant Staphylococcus aureus
    Nutrition Surveys
    Prevalence
    Staphylococcus aureus*
    Staphylococcus*
    Metrics
    Share
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