Prevalence and Associations of General Practice Registrars’ Management of Impetigo: A Cross-Sectional Analysis From the Registrar Clinical Encounters in Training (ReCEnT) Study

Background Impetigo is a mild bacterial skin infection of childhood that is usually managed empirically in primary care. Objective To establish the prevalence and associations of impetigo in general practice (GP) registrars’ consultations. Methods Cross-sectional analysis of the Registrar Clinical Encounters in Training (ReCEnT) study data. Results Impetigo was managed in 0.24% of problems and 0.43% of consultations. Patient variables associated with impetigo presentations were younger age and impetigo as a new problem, while patients with non–English-speaking backgrounds were less likely to present with impetigo. Associated registrar variables were being new to the registrar and practicing in outer regional/remote locations. Compared with all other problems/diagnoses, impetigo more often involved information seeking, ordering pathology, and prescription of medication, but less often involved follow-up or referral. Conclusions Impetigo accounts for 0.43 per 100 GP registrar consultations in Australia. Association with outer regional/remote areas may reflect climate and socioeconomic factors that predispose to impetigo. Associated pathology requests may reflect a lack of confidence in GP registrars’ management of impetigo. Cultural differences may exist regarding health-seeking behavior relating to impetigo.


Introduction
Impetigo is a common skin infection [1,2] caused by Staphylococcus aureus or Streptococcus pyogenes [2,3]. It is often seen in childhood and is associated with poverty and tropical environments [2] and is most prevalent in remote indigenous Australian children [2]. As a mild disease with good prognosis and potential for self-resolution [3], impetigo is managed in primary care [3,4], but because of its significant disease burden and highly contagious nature [2,3], empirical antibiotic treatment is recommended. Skin swabs for bacterial culture are reserved for severe/recurrent disease or empirical treatment failure [5,6]. Thus the management of impetigo has considerable implications for antibiotic stewardship.

Previous analysis from the Registrar Clinical Encounters in
Training (ReCEnT) study [7] raised questions regarding interpretation of Australian guidelines for impetigo management and the subsequent implications for antibiotic stewardship.
Characterizing the prevalence of impetigo and its associations is important to optimize and explore management that promotes antimicrobial stewardship.
Skin conditions are among the most common problems in Australian general practice (GP), managed in 17.4 per 100 encounters, and they account for 11.3% of problems [8].
Despite this frequency, studies have shown that registrars find skin conditions challenging and are not adequately prepared for the dermatology burden in the community [9]. Impetigo prevalence in global communities has been measured extensively, and while it is highest in remote Aboriginal and Torres Strait Islander populations, with a median prevalence Results: Impetigo was managed in 0.24% of problems and 0.43% of consultations. Patient variables associated with impetigo presentations were younger age and impetigo as a new problem, while patients with non-English-speaking backgrounds were less likely to present with impetigo. Associated registrar variables were being new to the registrar and practicing in outer regional/remote locations. Compared with all other problems/diagnoses, impetigo more often involved information seeking, ordering pathology, and prescription of medication, but less often involved follow-up or referral.
Conclusions: Impetigo accounts for 0.43 per 100 GP registrar consultations in Australia. Association with outer regional/remote areas may reflect climate and socioeconomic factors that predispose to impetigo. Associated pathology requests may reflect a lack of confidence in GP registrars' management of impetigo. Cultural differences may exist regarding health-seeking behavior relating to impetigo.

What Happens Differently During Impetigo Consultations?
Impetigo consultations were significantly shorter in duration (14 vs 19 minutes on unadjusted analysis and OR 0.94 per additional minute, 95% CI 0.93-0.96, P < 0.001 on multivariable analysis) and the registrars were more likely to seek help (OR 2.53, 95% CI 2.13-3.02, P < 0.001) ( Table 1). Of those who sought help from supervisors, the highest proportion were first-term registrars (70.7%) ( Table 2). The most frequent resource type used was electronic; the most common was Therapeutic Guidelines (61.65%) (Tables 2 and 3).

Discussion Prevalence
Impetigo accounted for 0.24% of problems seen by Australian GP registrars and was managed in 0.43 per 100 consul-

Consultation and Educational Variables
Consultation variables included duration, number of diagnoses/problems, pathology/imaging ordered, specialist referral made, follow-up organized, and medication prescribed. Educational variables included seeking information or assistance and generating learning goals.

Statistical Analysis
We conducted cross-sectional analysis of data from the ReCEnT cohort study performed on 16 rounds of 6-monthly collected data from 2010-2017, with analysis at the individual problem/diagnosis level.
The proportion of registrars' impetigo problems/diagnoses and the proportion of impetigo consultations were calculated, with 95% confidence intervals (CIs).

Impetigo vs Other Problems/Diagnoses
To test associations of a problem/diagnosis being impetigo,

Ethics Approval
The University of Newcastle Human Research Ethics Committee approved the study (Reference H-2009-0323).  Patients being more likely to present to the registrar with impetigo as a new problem or for the first time reflects impetigo's acute nature. Patients may be more willing to see registrars for acute issues or perceived minor problems [22]. Consultations for acute conditions are also booked on shorter notice, with the first doctor available, who is usually the registrar [9].
NESB patients were less likely to present with impetigo.
One-tenth of GP patients are from NESB [8] and 21% of Australians speak a language other than English at home [23].
Our finding may reflect cultural practices that predispose patients to impetigo; also as impetigo is a mild condition with the potential for self-resolution, this may reflect different cultural approaches to health-seeking behavior regarding impetigo.

Differences in Impetigo Consultations
Impetigo consultations were shorter; this is expected as impetigo is a common condition with a clinical diagnosis, systemically well patients [3,4], and clear guidelines available [6].
Registrars are more likely to seek information/assistance for impetigo despite its being a mild disease. First-term registrars were more likely to seek help from their supervisor than those in advanced terms, which may reflect initial inadequate preparation for the dermatological disease burden in the community [9], with confidence improving with experience.
The most commonly used resources were electronic (Table 2); the Therapeutic Guidelines [6] were most often used (Table   3). In impetigo consultations the majority of registrars (83%) did not generate learning goals, patients were mostly children, and medication was usually prescribed; therefore, registrars may have used this reference for dose checking rather than guidance on diagnosis/management.
tations. Finding comparable data regarding the prevalence of impetigo is difficult. The BEACH study grouped impetigo with other "skin problems," which were seen in 17.4 per 100 consultations [8]. In Aboriginal and Torres Strait Islander communities, impetigo encounters have been recorded as high as 7.5 per 100 consultations [14]. In a Dutch study, yearly impetigo incidence was 4 per 100 patients aged <18 years; however, the proportion of consultations was not measured [15]. Impetigo prevalence in global communities has been measured more extensively, although the majority of data was collected before 2010, with only 3 studies from 2010-2015 (3%) [2]. Impetigo prevalence is highest in remote Aboriginal and Torres Strait Islander populations with a median prevalence of 44.5% (IQR 34%-49.2%) [2]. A Canadian study of 2 First Nation communities found impetigo prevalence between 1% and 4.2% [16]; in comparison, the median prevalence of impetigo in Africa is 7% (IQR 4.1%-12.3%) [2] and 0.75% in Japan [17]. There is a paucity of prevalence data for North America, China, most European countries and non-Aboriginal Australian populations [2,18].

Impetigo Diagnosis Characteristics
Registrars working in outer regional/remote areas were more likely to see patients with impetigo. Impetigo is most prevalent in poorly resourced areas and tropical/arid climates [2]; the regional differences seen in our study may reflect lower income level and more tropical/arid climates [12,19] in Australian outer regional/remote areas.
Most patients with impetigo were <14 years, consistent with impetigo being a childhood disease [1,3]. Registrars see younger patients than do established GPs [8,20]; of registrar consultations, 17% involve patients <14 years [20,21] compared with 12% for established GPs [8]. Registrars are also more likely to see new patients, new problems, and acute illnesses [8], which may result in an elevated proportion of

Different Outcomes in Impetigo Consultations
Impetigo consultations were more likely to involve pathology being ordered, the majority being skin swabs for bacterial culture (Table 4), and medication prescription. As guidelines advise empirical treatment for impetigo, reserving skin swabs for severe, resistant, or recurrent disease [6], this may demonstrate lack of confidence with treating dermatological conditions. Follow-up and referrals were less likely in impetigo consultations, reflecting the mild nature of the disease and preferred management in primary care [3,4].

Strengths and Limitations
The strengths of this study are a large sample size of GP registrars with a high response rate from across Australia, including major cities and remote areas. A limitation of the analysis and interpretation of the data is the absence of information regarding the severity of impetigo. We are unable to account for this variable in our interpretation, and low numbers of Aboriginal and Torres Strait Islander patients (4%) means we were underpowered to analyze this variable.

Conclusions
Impetigo accounts for 0.43 per 100 consultations seen by Australian GP registrars. It is more common in outer regional/ remote/very remote areas and usually presents as a new problem. NESB patients are less likely to present with impetigo, which may reflect different cultural approaches to the management of a mild, potentially self-limiting condition.
Impetigo was associated with pathology being ordered, which may reflect a lack of confidence in Australian GP registrars when dealing with this presentation.