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Abstract

Introduction: Bacterial infection secondary to eczema and dermatitis occurs frequently. However, due to the inconvenience of clinical bacterial culture procedure, clinical diagnosis of bacterial infection following eczema is typically based on the appearance of skin lesions. To date, no surveys on the use of topical antibiotics for treating eczema and dermatitis in China have been carried out. Methods: The present study investigated the factors influencing the use of topical antibiotics to treat eczema and dermatitis in China. Logistic regression model and chi-square test were employed to examine whether topical antibiotics cause contact irritation. Results: It was found that the proportion of patients with eczema and dermatitis who were previously treated with topical antibiotics was 72.40%. The patients’ residence regions (southern vs northern territories, p < .001), hospital levels (secondary-level and below vs third-level hospitals, p = .004), itching degrees (no itching, itching does not require scratching, itching requires scratching, and scratching affects sleep and life quality, p < .001), skin infection status (no obvious infection phenomenon, possible infection, and clear infection, p = .001), and skin lesion infection severity (mild, moderate, and severe, p < .001) all showed statistically significant differences in the univariate analysis of antibiotic ointment treatment factors. The percentage of patients experiencing contact irritation reactions resulting from the use of topical antibiotics was 2.60%. The incidence of exposure to irritation was higher in patients who used more than two types of topical antibiotics compared to patients treated with only one type of topical antibiotic (% vs %, chi-square test, p < .001). Conclusion: The number of individuals who used topical antibiotics for eczema and dermatitis was relatively high in China. The degree of itching, infection possibility, and degree of skin lesion infection were positively correlated with the patients’ previous topical antibiotic treatment.

Keywords

eczema dermatitis bacterial infection topical antibiotics contact irritation

Introduction

Eczema is an inflammatory skin disease with obvious exudation tendency that can be caused by various internal and external factors.¹ Eczema is frequently accompanied by obvious itching, it can significantly lower patients’ life quality, and has a high reoccurrence rate.¹ Eczema has a prevalence of approximately 7.5% in the Chinese population and 10.7% in the United States.¹

Although eczema has existed for many years, its pathogenesis is still unclear. Currently, it is believed that eczema results from a comprehensive co-action of different internal and external factors, including abnormal immune function and skin barrier dysfunction.¹ Microorganisms can trigger or exacerbate eczema through direct invasion, superantigen action, or serious immune response induction.¹

Clinical manifestations of eczema can be divided into three stages, including the acute, subacute, and chronic phases. The acute stage is characterized by erythema and edema accompanied by large miliary papules, papules, blisters, erosions, and exudation, as well as unclear tissue boundary. In the subacute stage, the swelling and exudation are often decreased, and the erosion surface can be crusted and desquamated. In chronic eczema, rough hypertrophy, lichenification, and pigment changes may be present. In general, the rash is characterized by symmetrical distribution, high recurrence rate, and some subjective symptoms, such as mild or severe itching.

In the European guidelines for treatment of atopic eczema (atopic dermatitis) in adults and children treatment methods of eczema and dermatitis were recommended, which included patient perspective, general measures and avoidance strategies, basic emollient treatment, bathing, dietary intervention, topical anti-inflammatory therapy, phototherapy and antipruritic therapy, systemic immunosuppressive treatment, biological targeting treatment, microbial colonization and superinfection treatment, allergen-specific immunotherapy, psychosomatic counselling, and therapeutic patient education.² Besides topical emollients, the topical treatment of atopic eczema (atopic dermatitis) included the topical corticosteroids, topical calcineurin inhibitors, PDE4-inhibitor et al. Besides the traditional systemic treatments, dupilumab was approved the 6–11 age children, adolescent and adults with moderate–severe AD not controlled by topical therapies. JAK family consists of JAK1, JAK2, JAK3, and tyrosine kinase 2. The agents inhibiting JAK1 and/or JAK2, abrocitinib, baricitinib, and upadacitinib were currently approved for the treatment of patients with AD.^2–4

Previous studies have shown that microbial infection plays an important role in eczema and atopic dermatitis (AD) skin lesions, especially Staphylococcus aureus.⁵ In the acute phase of AD, microbial allergens and superantigens can bind to high-affinity IgE receptors on Langerhans cells in the epidermis, resulting in a series of allergic reactions, such as amplified eosinophil reactivity.⁶ However, there is currently no standard or expert consensus for the topical antibiotic treatment of eczema and dermatitis. In addition, antibiotic use in the Chinese population requires a thorough investigation. The present study explored the use and influencing factors of topical antibiotics for eczema and dermatitis treatment in China.

Materials and methods

To understand the use of topical antibiotics by dermatologists in China for treating eczema and dermatitis, a multi-center cross-sectional study entitled “Survey on the Application and Allergies of Topical Antibiotics” was carried out between December 2019 and May 2020. This study was approved by Ethics Committee of Beijing Friendship Hospital, Capital Medical University. All experiments were performed in accordance with relevant guidelines and regulations. Verbal informed consent was obtained from each participant. A total of 83 Chinese hospitals located in 24 provinces and municipalities across the country participated in this research project. The analyzed study data included information on patients’ age at disease onset, course of disease, degree of pruritus, medical history, manifestations and severity of skin lesions, antibiotic ointment types used in the past, presence of itching when using the antibiotic ointment, redness and swelling, and patients’ current treatment status. A total of 6000 questionnaires were distributed in the survey, with 5340 patients agreeing to participate. The response rate was 89.0%.

The information collected from the questionnaire was manually entered into an Excel sheet and SPSS (IBM SPSS Statistics 26) was used to perform the data analysis. The constituent ratio of categorical variables was calculated and chi-square test was used to compare the rank and sort variables based on statistical differences. In the logistic regression analysis model, the antibiotic ointment treatment was the dependent variable, while the independent variables included patient residence regions, age, sex, hospital levels, itching degree, lesion infection, skin lesion infection severity, and degree of pruritus.

Results

Demographics

The total number of registered patients was 5340 in the present study. With the missing data points excluded, there were 2243 male and 2355 female patients (with a sex ratio of 1:1.05). The patients’ age ranged from 19 days to 95 years, with an average age of 36.53 years and a median age of 35 years. In terms of the regional distribution, 2080 and 2518 patients were from the southern and northern provinces of China, respectively. A total of 3763 patients within the sample were registered with tertiary hospitals, while 687 patients were treated at secondary and lower-level hospitals. The demographic characteristics of the study population are summarized in Table 1.

Table 1.

Study population demographics.

	Classification	No (n. %)
Sex	Male	2243 (48.78)
Sex	Female	2355 (51.22)
Age group (years)	0∼	317 (6.89)
	2∼	629 (13.68)
	12∼	195 (4.24)
	18∼	2561 (55.70)
	60∼	896 (19.49)
Region	South	2080 (45.24)
Region	North	2518 (54.76)
Hospital levels	Secondary and lower	687 (14.94)
Hospital levels	Tertiary	3763 (81.84)

Total topical antibiotic use

The present study excluded 33 patients who did not provide information about past topical antibiotics use and then further eliminated 10 patients who previously used medication other than topical antibiotics. Overall, 72.40% of all patients were previously treated with topical antibiotics. The top five most frequently used topical antibiotics were erythromycin ointment (1030 cases, 26.86%), fusidic acid cream (757 cases, 19.74%), mupirocin ointment (730 cases, 19.04%), compound polymyxin B ointment (544 cases, 14.19%), and miconazole nitrate cream (510 cases, 13.30%). The percentage of patients who have used topical antibiotics compared to that of patents who have not and the data for the top five most frequently used topical antibiotics are presented in Figures 1 and 2, respectively.

Figure 1.

The percentage of patients who have used versus have not used topical antibiotics.

Figure 2.

The top five most frequently used topical antibiotics and their accumulated proportion.

According to the prescription information provided in the 5187 questionnaires, 1975 patients were prescribed antibiotics (38.08%). There were 62 types of prescribed antibiotics, including traditional Chinese medicine-based topical antibiotics and systemically applied antibiotics. The top five drugs were compound polymyxin B ointment (528 cases, 243.2%), fusidic acid cream (471 cases, 217.0%), triamcinolone acetonide econazole cream (273 cases, 138.2%), mupirocin ointment (156 cases, 71.9%), and compound ketoconazole cream (79 cases, 35.4%).

Univariate analysis of antibiotic ointment use

Analysis of factors affecting antibiotic ointment use showed that five variables (region, hospital level, degree of pruritus, lesion infection, and lesion infection severity) out of seven (region, hospital level, age, gender, degree of pruritus, lesion infection, and lesion infection severity) showed statistically significant differences (Table 2). Patients’ age and gender did not affect the use of antibiotic ointment (Table 2).

Table 2.

Assessment of key factors that might influence antibiotic ointment use.

Variable	Classification	No (n. %)	Topical antibiotics no (n. %)	χ²	p-value
Region	South	2080 (45.24)	1617 (77.74)	41.643	0.000
Region	North	2510 (54.76)	1744 (69.26)
Hospital level	Secondary and lower	771 (16.80)	531 (68.87)	8.410	0.004
Hospital level	Tertiary	3827 (83.20)	2830 (73.95)
Age group (years)	0∼	317 (6.89)	222 (70.03)	3.056	0.548
	2∼	629 (13.68)	465 (73.93)
	12∼	195 (4.24)	149 (76.41)
	18∼	2561 (55.70)	1876 (73.25)
	60∼	896 (19.49)	649 (72.43)
Sex	Male	2243 (48.78)	1650 (73.56)	0.482	0.488
Sex	Female	2355 (51.22)	1711 (72.65)
Itching degree	No itch	246 (5.35)	138 (56.10)	44.501	0.000
	Light, not scratching required	620 (13.48)	435 (70.16)
	Scratching required	230 (50.02)	1707 (74.22)
	Scratching required, affecting sleep and living quality	143 (31.14)	1081 (75.49)
Infection of lesions	No obvious infection	343 (74.62)	2460 (71.70)	13.984	0.001
	Possible infection	964 (20.97)	740 (76.76)
	Clear infection	203 (4.41)	161 (79.31)
Severity of skin lesion infection	Mild	241 (52.44)	1701 (70.55)	17.039	0.000
	Moderate	1752 (38.10)	1325 (75.66)
	Severity	435 (9.46)	335 (77.01)

Chi-square test.

In addition, the key factors that might influence the antibiotic ointment use were analyzed using the logistic regression model. The antibiotic ointment treatment was the dependent variable, while the independent variables included patients’ residence regions, hospital levels, degree of pruritus, lesion infection, and lesion infection severity. Stepwise regression method showed that the inclusion criterion was 0.1 and the exclusion criterion was 0.05. These results are summarized in Table 3.

Table 3.

OR estimation for selected variables.

Variables	Coefficient	Wald $χ^{2}$	p-value	OR	OR 95% CI
Region	−0.414	36.182	0.000	0.661	(0.578, 0.756)
Hospital level	0.175	3.990	0.046	1.191	(1.003, 1.413)
Itching degree	0.191	20.348	0.000	1.211	(1.114, 1.316)
Infection of lesions	0.180	7.581	0.006	1.198	(1.053, 1.362)
Degree of skin lesion infection	0.104	3.576	0.059	1.109	(0.996, 1.235)

Parameter tests and WALD tests.

Occurrence of adverse irritation reactions with topical antibiotic use

Among the 5308 patients who listed adverse reactions associated with the use of topical antibiotics, 138 patients reported itching, redness, swelling, or burning irritation (accounting for 2.60%). In addition, the top five topical antibiotics that caused irritation reactions included miconazole nitrate cream (27 cases, 5.29%), mupirocin ointment (35 cases, 4.79%), compound polymyxin B ointment (22 cases, 4.04%), erythromycin ointment (28 cases, 2.72%), and fusidic acid cream (18 cases, 2.38%). After excluding 11 patients who did not disclose gender or age information, there were 57 male and 80 female patients (1:1.40 ratio, age range: 3 months to 80 years, average age of 34.78 years) who experienced irritation reactions following previous topical antibiotic treatments. Among the 138 patients with irritation reactions to antibiotics, patients who had skin lesions with exudate, pus or pustular lesions, erosions, blisters, chapped skin lesions, and none of the above accounted for 14.5%, 7.2%, 1.4%, 11.6%, and 63.8%, respectively.

In addition, to determine the effects of topical antibiotic ointment types on adverse reaction rates, 3835 patients who used topical antibiotics, 3497 patients who used one topical antibiotic (91.19%), 237 patients who used two topical antibiotics (6.18%), and 101 patients who used three or more kinds of topical antibiotics (2.61%) were analyzed. The incidence of irritation reactions after using one topical antibiotic was 2.97%. It was 8.77% after using two kinds of topical antibiotics and 9.90% after using three or more kinds of topical antibiotics. The chi-square value of the contingency table was 35.08, p < .01, indicating a statistically significant difference in the incidence of adverse reactions among the groups. Further pairwise comparison was conducted and the Bonferroni method was used to correct the p-value. After hypothesis testing, the incidence of adverse reactions in patients using one type of topical antibiotic was lower than that in patients using two types of topical antibiotics. The chi-square value was 23.77, p < .01 < .0167. The incidence of adverse reactions in patients using one type of antibiotic was lower than that in patients using three or more types. The chi-square value was 13.18, p < .01 < .0167 (Table 4).

Table 4.

Adverse reaction rates for different types of topical antibiotic ointments.

Types	No (n. %)	Rate(%)	p-value^a
1	3497 (91.19%)	2.97	< .01
2	237 (6.18%)	8.77
3 and more	101 (2.61%)	9.90

^aThere was no statistically significant difference in the incidence of adverse reactions between patients using two types of antibiotics and those using three or more types (chi-square value 0.092, p > .05 > .0167).

Discussion

S. aureus can colonize 80%–100% of skin lesions in eczema and AD patients. In contrast, S. aureus can only be isolated from 5% to 30% of the abraded skin biopsies of healthy individuals.^7–10 In addition, a positive correlation was found between eczema/skin inflammation severity and S aureus colonization density.^9,11,12 Moreover, bacterial colonization was identified as an important mechanism for aggravating skin lesions.^9,11,12

There are some contradicting results in the previously published studies investigating the effects of antimicrobial therapy on S. aureus colonization and skin inflammation severity.¹³ In several double-blind placebo clinical trials, administration of topical and systemic antimicrobials was shown to be effective in reducing S. aureus colonization density and improving skin lesion healing outcomes.^6,11 However, oral antibiotic treatments did not significantly improve AD in two double-blind placebo studies.^14,15 Furthermore, topical antimicrobials combined with steroids were recommended for treating eczematous dermatitis.⁴

Hagino et al. found lower responsiveness of head-and-neck rash to upadacitinib treatment. They also identified several factors that can contribute to treatment resistance of head-and-neck erythema, particularly abundant head and neck colonization by Malassezia furfur.⁴

Guidelines for Diagnosis and Treatment of Eczema in China (2011) have pointed out that bacterial infection and colonization can often induce or aggravate eczema. Therefore, the proper use of antibiotics is of vital importance for treating eczema and dermatitis. Various topical antibiotic preparations can be used together with different kinds of glucocorticoids.¹ In addition, based on the Overview of Chinese and Foreign Diagnosis and Treatment Guidelines for Hand Eczema (published in 2019), when eczema is complicated by bacterial infection, topical antibiotic preparations or combined antibiotic and glucocorticoid therapeutic regimen can be used for anti-infection treatment.¹⁶ However, there is an increased risk of S. aureus colonization in AD skin lesions according to the Antimicrobial Treatment Guidelines for the Diagnosis and Treatment of Atopic Dermatitis in China (2020). Topical glucocorticoids, topical calcineurin inhibitors, and 0.005% bleaching powder bath can lower the colonization rate of S. aureus. In addition, short-term systemic or topical antibiotics can be prescribed when symptoms are obvious. It has been reported that systemic antibiotics can be selected from penicillin or first-generation cephalosporins according to drug susceptibility results, with the course of treatment lasting for 1–2 weeks (similar to the treatment period of topical antibiotics). However, prolonged antibiotic treatment can frequently lead to drug resistance and allergies.¹⁷

In the present study, it was found that the percentage of patients with eczema and dermatitis with previous topical antibiotic use was high (72.40%), which may be related to the recommendation in the “Chinese Eczema Diagnosis and Treatment Guidelines (2011)” stating that multiple types of topical antibiotics can be used to treat eczema. However, only 38.08% of patients used topical antibiotics during this visit, which could be associated with the efforts to eliminate clinical antibiotic abuse, antibiotic resistance issues, and irritant contact dermatitis resulting from topical antibiotic use.

In addition, it was demonstrated that the patients’ residence regions (southern vs northern territories, p < .001), hospital levels (secondary-level and below vs third-level hospitals, p = .004), itching degrees (no itching, itching does not require scratching, itching requires scratching, and scratching affects sleep and life quality, p < .001), skin infection status (no obvious infection phenomenon, possible infection, and clear infection, p = .001), and skin lesion infection severity (mild, moderate, and severe, p < .001) all showed statistically significant differences in the univariate analysis of antibiotic ointment treatment factors. However, patients’ age and gender did not affect the use of topical antibiotics.

Moreover, the key factors that could influence the antibiotic ointment use were analyzed using the logistic regression model. The antibiotic ointment treatment was the dependent variable, while the independent variables included residence regions, hospital levels, degree of pruritus, lesion infection, and lesion infection severity. Specifically, it was found that the OR value in the region was 0.661, indicating that hospitals in the northern regions were 0.661 times more likely to use antibiotics than those in the southern territories. The OR value at the hospital level was 1.191, suggesting that patients registered at tertiary hospitals were 1.191 times more likely to use antibiotics than those at secondary and lower-level hospitals. The degree of itching was 1.211, which meant that whenever the degree of itching increased by one, the possibility of using topical antibiotics increased 1.211 times, with all other factors remaining unchanged. For example, the data indicated that patients who experienced light itching but no scratching were 1.211 times more likely to use topical antibiotics than patients without itching. Furthermore, the OR value for skin lesion infection was 1.198, meaning that the possibility of using antibiotic ointment was 1.198 times more for one-unit increase in skin lesion infection condition. More specifically, it suggested that patients with possible skin lesion infection were 1.198 times more likely to use topical antibiotics than those without obvious infection. Patients with obvious skin lesion infection were 1.198 times more likely to use topical antibiotics than patients with possible skin lesion infection. Finally, the OR value for the severity of skin lesion infection was 1.109, indicating that the likelihood of using antibiotics for every increase in skin lesion infection severity was 1.109 times that of the original. Specifically, patients with moderate lesion infection severity were 1.109 times more likely to use antibiotics than patients with mild lesion infection severity.

Moreover, the side effects of using topical antibiotics, such as itching, redness, swelling, and burning, were investigated using a questionnaire. The total incidence of side effects was 2.60%, and the highest incidence of 5.29% was noted for miconazole nitrate cream. In addition, among the patients with irritation reactions to topical antibiotics, those who experienced skin lesions with exudate, pus or pustular lesions, erosions, blisters, chapped skin lesions, and none of the above accounted for 14.5%, 7.2%, 1.4%, 11.6%, and 63.8% of the total cohort, respectively. Overall, the incidence of itching, redness, swelling, and burning irritation symptoms with topical antibiotic treatments was low. Therefore, the side effects of using topical antibiotics may not have an obvious impact on patient treatment.

Furthermore, among the 3835 patients who used topical antibiotics, those who used one, two, and three or more types of topical antibiotics accounted for 91.19% (3497 cases), 6.18% (237 cases), and 2.61% (101 cases) of the cohort, respectively. The incidence of irritation reactions after using one, two, and three or more types of topical antibiotics was 2.97%, 8.77%, and 9.90%, respectively. It should be noted that significant difference was observed in the incidence of irritation reactions after using one compared to two or more types of topical antibiotics (p < .001). However, there was no significant difference in the incidence of irritation reactions between two and three types of topical antibiotics (p = .744). The data suggested that increasing the number of topical antibiotic types used may lead to a higher risk of skin irritation.

Several limitations should be considered when interpreting the study results. The power analysis for sample size calculation was not carried out due to limited conditions. This was a hospital-based study, selective bias was inevitable due to nonhomogeneous population and differential spatial distribution. All of these factors may have resulted in unavoidable bias.

Conclusion

More than 5000 patients from 83 hospitals across China participated in this research project, covering different regions and hospital levels. Factors affecting the use of topical antibiotics to treat eczema and dermatitis in China were investigated.

According to the present study, the number of patients who used topical antibiotics for eczema and dermatitis was relatively high (72.40%). The degree of itching, infection possibility, and degree of infection in skin lesions were positively correlated with patients’ previous topical antibiotic treatment condition. In addition, the percentage of patients with eczema and dermatitis seeking treatment in hospitals was higher in the southern cities compared to the northern territories. Interestingly, the proportion of patients pursuing topical antibiotic treatments in tertiary hospitals was also higher than that in secondary and lower-level hospitals.

In addition, the incidence of itching, redness, and burning irritation symptoms caused by topical antibiotic use was relatively low. Adding more types of antibiotic ointments for eczema and dermatitis treatment can significantly increase the irritation risks. Based on these findings, simultaneous use of multiple types of topical antibiotics is not necessary and can cause more irritation side effects. Therefore, these results are of vital importance for guiding the use of topical antibiotics to treat eczema and dermatitis more effectively in future clinical work.

Supplemental Material

Supplemental Material - An investigation on the use of topical antibiotics for treating eczema and dermatitis in China

Supplemental Material for An investigation on the use of topical antibiotics for treating eczema and dermatitis in China by Juan Shao, Xin Wang, Zhongwen Zhang and Linfeng Li in European Journal of Inflammation.

Footnotes

Acknowledgements

We thank the dermatologists from the 83 participating hospitals. We also thank the associate editors and the reviewers for their feedback that improved this paper.

Author contributions

Conceptualization, Linfeng Li; data analysis and original draft preparation, Juan Shao; manuscript review and editing, Xin Wang; data analysis, Zhongwen Zhang. All authors have read and approved the published version of the manuscript.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Ethical statement

ORCID iDs

Juan Shao

Xin Wang

Linfeng Li

Supplemental Material

Supplemental material for this article is available online.

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