Impetigo incidence and treatment: a retrospective study of Dutch routine primary care data - Julius Center
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Family Practice, 2018, 1–7
doi:10.1093/fampra/cmy104
Epidemiology
Downloaded from https://academic.oup.com/fampra/advance-article-abstract/doi/10.1093/fampra/cmy104/5139618 by guest on 20 October 2018
Impetigo incidence and treatment: a
retrospective study of Dutch routine primary
care data
Madelyn E N Loadsmana,b, Theo J M Verheijc and Alike W van der Veldenc,*
School of Medicine, Griffith University, Brisbane, Australia, bLogan Hospital, Queensland Health, Queensland,
a
Australia and cJulius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, The
Netherlands.
*Correspondence to Alike W van der Velden, Julius Center for Health Sciences and Primary Care, University Medical Center
Utrecht, STR 6.103, Heidelberglaan 100, 3584 CX Utrecht, The Netherlands; E-mail: a.w.vandervelden@umcutrecht.nl
Abstract
Background. There is a lack of recently published data on impetigo presentation incidence and
treatment practices in the routine Western European primary care setting.
Objectives. To investigate impetigo incidence, treatments and recurrence in primary care in the
Netherlands.
Methods. A retrospective, observational study. Electronic records of patients treated for impetigo
in 2015 at 29 general practices in Utrecht and surrounds were reviewed. An episode of impetigo was
defined as one or more patient–doctor contacts within 8 weeks of the index consultation. Within
an episode, patient demographics and prescribing patterns were analysed including number of
treatments, and the category and sequence of individual medicines.
Results. A total of 1761 impetigo episodes were managed, with an incidence rate of 13.6 per 1000
person years. Impetigo peaked in summer. Most patients, the majority children, experienced a
single episode (93%), and 25% had eczema as comorbidity. Topical antibiotics (primarily fusidic
acid) were the most prescribed initial treatments (85%), followed by oral antibiotics (14%). Topical
antibiotics were progressively used less over subsequent treatments, while there was an inverse
increase in oral antibiotic use. Topical fusidic acid as the most common first line treatment seemed
satisfactory as only 12% of initial treatments with this drug received further therapy. Repeat
treatments generally occurred within 7 days.
Conclusion. This study of impetigo prescribing patterns in primary care highlighted that Dutch
general practitioners were generally adherent to national treatment guidelines. Topical treatment,
and if needed systemic small-spectrum antibiotic treatment, appeared satisfactory; these findings
aid in antimicrobial stewardship.
Key words: Antibacterial agents, epidemiology, fusidic acid, general practice, guideline adherence, impetigo, skin infection.
Introduction cases persist for several weeks. Treatment is often initiated to
reduce the duration and spread of infection (1,3,4). In addition,
Impetigo is a contagious superficial bacterial skin infection com-
impetigo can have serious consequences, as it is associated with
monly associated with Staphylococcus aureus, group A beta-
post-infectious glomerulonephritis and cellulitis, especially in cer-
haemolytic Streptococcus pyogenes, or both (1,2). Although
tain specific populations (2,5,6).
impetigo can be self-limiting, resolving without intervention, some
© The Author(s) 2018. Published by Oxford University Press. All rights reserved.
1
For permissions, please e-mail: journals.permissions@oup.com.2 Family Practice, 2018, Vol. XX, No. XX
While the incidence of impetigo is assumed to be high in gen- • Oral antibiotics: Doxycycline J01AA02, Amoxicillin
eral practice, previously reported incidence rates vary between geo- J01CA04, Pheneticillin J01CE05, Flucloxacillin J01CF05,
graphic locations and time periods (7–10). Despite location and Amoxicillin/Clavulanic acid J01CR02, Trimethoprim J01EA01,
time-point differences, the global burden of impetigo is estimated Sulfamethoxazole and Trimethoprim J01EE01, Erythromycin
to be over 100 million people affected worldwide at any one time J01FA01, Clarithromycin J01FA09, Azithromycin J01FA10,
(5,11). Although impetigo affects people of all ages, it is especially Clindamycin J01FF01, and Nitrofurantoin J01XE01
frequent in children aged 1 to 4 years (1,12). The condition affects • Topical antibiotics: Tetracycline D06AA04, Fusidic acid
the whole family. While it is difficult to determine the exact societal D06AX01 and Mupirocin D06AX09
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burden of impetigo, it can be reasoned that there are costs associated • Antiseptics: Chlorhexidine D08AC02
with treatment, lost productivity and imposed social isolation (2). • Topical products: Zinc cream D02AB
There are a variety of common treatment options for impetigo,
including topical antibiotics (mupirocin, fusidic acid), systemic anti-
biotics (penicillins, such as flucloxacillin and amoxicillin/clavulanic Data, outcomes and analysis
acid, cefalosporins and macrolides) and topical antiseptics (chlo- The impetigo episode profile was determined by analysing the total
rhexidine and povidone iodine) (1,13). Given the problems related number of episodes, number of contacts within an episode, distribu-
to antimicrobial resistance, it is important to gain insight into what tion of single compared with multiple episodes, the number of weeks
treatment options are used and which ones appear to be satisfac- between first and last GP contact, season of episode occurrence and
tory with respect to effectiveness, symptom duration and preven- overall episode incidence rate. Within the impetigo episodes, treat-
tion of recurrence. Such insight is key in antimicrobial stewardship ment prescribing patterns were analysed: number and category
and could aid in reducing impetigo treatment with systemic and/or of treatments, most commonly prescribed individual medicines,
broad-spectrum antibiotics (14). By using a systematic approach to treatment sequence and time intervals between treatments. Finally,
promote judicious antimicrobial prescribing, there is potential to patient-related factors that may have contributed to multiple episode
reduce emergence of resistance, as well as reduce costs and other recurrence were assessed. Analyses were conducted using IBM SPSS
adverse effects associated with inappropriate use. There is limited Statistics Version 21 and Excel 2010.
recent data on treatment practices in an average primary care set- As data were originally collected for routine health service,
ting in Western Europe, as evidenced by a literature review of pub- research was conducted and reported in accordance with the
lications within the last 5 years using the PubMed database and REporting of studies Conducted using Observational Routinely-
the search terms impetigo and anti-bacterial agents. Our study, collected health Data (RECORD) guideline (17).
therefore, aimed to investigate the incidence of impetigo presen-
tation, treatments used and recurrence in a primary care setting.
Information on these issues is pivotal to development of pragmatic, Results
evidence-based guidelines to effectively manage impetigo patients Patients and episodes
in the community.
In 2015, 1761 episodes of impetigo (129 844 person years) were
managed by GPs. Among these patients, there was an approximately
Methods even sex distribution and a larger percentage of younger children. In
a quarter of episodes, patients had recorded eczema as a comorbid-
Design, setting and patients ity, with lower percentages found for hay fever and asthma. The vast
We conducted a retrospective, observational study of patients majority of patients (93%) experienced a single episode in 1 year.
treated for impetigo in primary care. Data were obtained from 29 The majority of episodes (78%) had one patient–doctor contact.
practices within the Julius General Practitioners Network Database, And, concomitantly, 86% of impetigo episodes had a time window
a database of routine primary care data of all patients from 45 prac- between diagnosis and last contact of 1 to 7 days. The diagnosis
tices located in the Dutch city of Utrecht and its surrounding areas. of impetigo appeared to have seasonal variation, with 29.5% diag-
Practitioners in these centres are experienced in using International nosed in summer compared with 19.6% in spring (Table 1).
Classification of Primary Care (ICPC) codes as part of electronic
patient record keeping (15). A total of 139 860 patient records
Episode incidence
(129 844 person years) were searched for doctor–patient contacts
The overall incidence rate of impetigo episodes, including single and
resulting in a diagnosis of impetigo, using the ICPC code S84. When
subsequent ones that presented to GPs was 13.6 per 1000 person
patients visited the general practitioner (GP) on more than one occa-
years, with a threefold higher rate (40 per 1000 person years) for
sion for impetigo, contacts within an 8-week period were combined
children under 18 years. The incidence rate was highest in children
into an episode. Within an episode, several treatments could be pre-
aged 0–6 years (64.6 per 1000 person years) and progressively
scribed. Records from 1 January to 31 December 2015 were screened
declined with increasing age to 6.2 per 1000 person years for adults
for S84 contacts, which was extended for 8 weeks in 2016 for epi-
(≥18 years).
sodes initially diagnosed in December 2015 to obtain data reflecting
one complete year. Patient demographic data were extracted: age,
sex and atopic comorbidities asthma (R96), hay fever (R97) and Treatment
eczema (S87). The continuous variable age was categorized in 0–6 Of 1761 impetigo episodes, 1542 (87.6%) received GP-prescribed
(=0–Impetigo incidence and treatment in primary care 3
most frequent choice (14%). Where more than one treatment was oral flucloxacillin (10.4%). With subsequent treatments, treatment
received during an episode, there was an increasing trend in pre- with fusidic acid decreased, whereas the relative contribution of
scribing oral compared with topical antibiotics. Contribution of mupirocin increased. Furthermore, flucloxacillin and azithromycin
antiseptics and zinc was low. Figure 2 shows the specific medica- were often used as second or third treatments, whereas amoxicil-
tion sequentially prescribed. Topical fusidic acid was the most com- lin with or without clavulanic acid was used as third or fourth
monly prescribed initial treatment (n = 1245, 80.7%), followed by treatments.
Table 1. Impetigo patient (n = 1637) and episode (n = 1761) charac-
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Time intervals and treatment sequence
teristics from the Dutch JHN database (2015)
Of the 1542 treated episodes, 1497 (97%) received treatment on the
Characteristics of patients and episodes % day of diagnosis and 28 (1.8%) within 7 days. Although only in a
small proportion of episodes multiple treatments were given, more
Sex Male/female 47.4/52.6
than half of episodes receiving additional treatment had their sub-
Age 0–6 years 41.6
sequent treatment within 7 days. Treatment sequences are shown in
7–17 years 22.4
18–65 years 31.1 Figure 3. Fusidic acid was prescribed as initial treatment in 1245
≥66 years 3.9 episodes (80.7%). This treatment appeared satisfactory, as only
Comorbidity Hay fever 10.5 a small proportion of cases received further treatment (n = 145,
Eczema 25.1 12%). Of these, flucloxacillin was the most commonly prescribed
Asthma 13.5 second treatment, followed by a second course of fusidic acid, or
Episodes Single (1st episode) 93 a broad-spectrum oral antibiotic. In contrast, initial flucloxacillin
Recurrent (2nd to 4th 7 therapy resulted in only 93 episodes (58%) receiving no further
episodes)
therapy. As a second treatment, fusidic acid was most often pre-
Time from diagnosis to last 1 week 85.7
scribed, followed by a second course of flucloxacillin, or a broad-
contact 2–3 weeks 7.4
spectrum antibiotic.
4–8 weeks 6.9
Patient contacts within an 1 78.4
episode 2 14.5 Single and multiple episodes in one year
3 5 There were 124 recurrent episodes (7%) where patients experi-
4–7 2.1 enced a second, third or fourth impetigo episode in the same year.
Seasonal variation Winter 24.3
The number of GP contacts for these single and subsequent epi-
Spring 19.6
sodes had a similar distribution. Recurrent episodes of impetigo
Summer 29.5
seem to occur more frequently in young patients and in patients
Autumn 26.6
with eczema (Table 2).
84.9
90
80
70
58.2
60
49.8
PERCENTAGE (%)
47.5
50
50
50
40
40
30
14.4
20
10
2.3
1.8
0.5
0.4
0.2
0
0
0
0
INITIAL TREATMENT SECOND TREATMENT THIRD TREATMENT FOURTH TO SIXTH
N=1542 N=259 N=55 TREATMENTS N=22
TREATMENT NUMBER AND CATEGORY
Oral An bio c Topical An bio c Topical An sep c Topical Zinc Barrier
Figure 1. Treatment choice for impetigo by medication category from initial to sixth treatment in Dutch primary care (2015). Of 1761 episodes, a total of 1542
received treatment. The relative contribution of oral antibiotic, topical antibiotic, topical antiseptic and topical zinc treatments are shown for the first, second,
third and fourth to sixth treatments.4 Family Practice, 2018, Vol. XX, No. XX
90
80.7
80
70
60
PERCENTAGE (%)
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50
41.7
40
32.7
31.3
29.1
29
30
18.8
14.6
20
12.5
12.5
12.5
10.4
9.1
9.1
7.3
7.3
10
4.3
1.2
1.2
4
0
0
0
0
0
FUSIDIC ACID FLUCLOXACILLIN MUPIROCIN AMOXICILLIN AZITHROMYCIN AMOXICILLIN
(TOPICAL) (TOPICAL) AND CLAVULANIC
ACID
TREATMENT
Ini al Treatment n=1542 Second Treatment n=259 Third Treatment n=55 Fourth Treatment n=16
Figure 2. The most frequently prescribed specific medication for impetigo from initial to fourth treatment. The relative contribution of specific medication
prescribed for patients with impetigo is shown for the first, second, third and fourth treatments for Dutch primary care in 2015.
Discussion individual patient contacts into disease episodes over seventeen hun-
dred episodes were identified, allowing longitudinal mapping of the
Summary of principal findings
epidemiology of impetigo and analysis of successive prescriptions
Investigating the current presentation incidence of impetigo and its within episodes. This paper, therefore, describes the current routine
treatment in primary care is important in understanding the impact management of impetigo in everyday general practice and, further-
this infection has on the community, for comparing treatment prac- more, allows the evaluation of adherence to treatment guidelines.
tice with existing guidelines, and for antimicrobial stewardship. This While studies often report prevalence, we also captured patients
study provides such data. It highlights that impetigo occurs widely in experiencing first and recurrent episodes of impetigo within the year.
the community, with incidence rates highest in children. Our patient However, there were also some limitations to this study. We have
profile was a young child who experienced a single occurrence, most worked with data captured retrospectively from routine health care
often in summer. From diagnosis to last contact, such patients often provision, which are less comprehensive than those available in pro-
had only one to two GP visits, and were treated satisfactorily with spective research. Information about the severity, extension of the
topical fusidic acid. Oral treatment was used in increasing frequency symptoms and lesions, and the specific reason for a subsequent con-
when second, or third treatments were given, with subsequent pre- sultation would have facilitated analyses concerning effectiveness
scriptions usually written within 7 days. Patients experiencing mul- of prescribed medication, the appropriateness of treatment choice,
tiple impetigo infections were more likely to be young children and/ or at which point and/or why it was deemed necessary to change
or suffering from eczema. treatments. In addition, there were no microbiological data on anti-
bacterial sensitivities available; this would have enabled the relation-
Strengths and limitations ship between resistance and subsequent treatments to be examined.
The main strength of this study was a database of patients from Although recorded as infrequently prescribed, the actual use of anti-
multiple general practices, with a population well representative of septics and topical zinc is probably underestimated as these products
a (sub)urban western European primary care setting. We therefore are available over the counter without a prescription and could have
consider the general characteristics of impetigo disease representative also been recommended by the GP. Finally, while the database was
for this setting. However, as patients’ health care seeking behaviour able to determine the provision of a subsequent treatment, there was
and guidelines vary between European countries, the GP presenta- no way to determine whether the patient ceased the previous treat-
tion incidence and treatment characteristics we presented are gen- ment, or was concomitantly using more than one therapy. For future
eralizable to the Dutch setting. These can nevertheless be used to studies, GPs’ registration of infection severity and/or other consid-
inform and raise awareness in other countries with respect to the use erations is recommended; capturing these parameters will further
of topical and small-spectrum antibiotics for impetigo. By combining deepen insight.Impetigo incidence and treatment in primary care 5
Ini al Tx Ini al Tx
Fusidic Acid Flucloxacillin
n=1245 n=160
No 2nd Tx No 2nd Tx
n=1100 (88%) n=93 (58%)
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2nd Tx 2nd Tx
n=145 (12%) n=67 (42%)
FA BS FC MU OTH FA BS FC MU OTH
n=35 n=25 n=61 n=12 n=12 n=41 n=11 n=7 n=3 n=5
(24%) (17%) (42%) (8%) (8%) (61%) (16%) (10%) (4%) (7%)
3rd Tx 3rd Tx 3rd Tx 3rd Tx 3rd Tx 3rd Tx 3rd Tx 3rd Tx
N: 69% N: 68% N: 74% N: 83% N: 90% N: 73% N: 100% FA: 100%
FC: 17% FC: 20% FA: 11% FC: 8% FA: 7% FA: 9%
FA: 6% FA: 4% BS: 8% MU: 8% MU: 3% BS: 9%
BS: 6% BS: 8% FC: 3% OTH: 9%
MU: 3% MU: 2%
OTH: 2%
Figure 3. Comparison of treatment sequence for impetigo where initial therapy was fusidic acid, or flucloxacillin (Dutch primary care, 2015). Of patients initially
treated with FA or FC, their subsequent treatments are shown in absolute numbers and percentages. Tx = treatment; NT = no treatment; FA = fusidic acid;
BS = broad-spectrum (amoxicillin, amoxicillin plus clavulanic acid, azithromycin); FC = flucloxacillin; MU = mupirocin; OTH = other treatments.
Table 2. Comparison of single and recurrent episodes of impetigo care studies (7–10). A previous Dutch study found impetigo rates
(n = 1761) with respect to the number of patient contacts, patient in children had increased over time, from 16.5 to 20.6 per 1000
age and comorbidities (Dutch JHN database, 2015) patient years in 1987 to 2001 (10). The high incidence rates in
children could be explained by an increased pressure on parents
Single episodes Recurrent episodes
to seek treatment, to avoid exclusion of obviously infected chil-
n % n % dren from school (18). Other contributing factors include increas-
ing virulence and emergence of S. aureus carrying drug resistance
Episodes 1637 93 124 7 genes (19,20).
Contacts
Most impetigo episodes occurred in summer. Several studies
1 1281 78.3 99 79.8
have found seasonal variation in impetigo infections, with a higher
2 239 14.6 17 13.7
3 83 5.1 5 4.0
frequency seen in warmer months (21). In our cohort, a quarter
4 to 7 34 2.1 3 2.4 of patients with single episodes and almost a third with recurrent
Age episodes also suffered from eczema. This co-occurrence is consist-
0–6 years 674 41.2 59 47.6 ent with a population-based study of 913 children, which found a
7–17 years 367 22.4 28 22.6 lifetime impetigo prevalence higher in children with atopic derma-
≥18 years 596 36.4 37 29.8 titis (22). Defects in skin immune surveillance mechanisms, such
Comorbidities as decreased production of antimicrobial peptides and expression
Asthma 223 13.6 14 11.3 of functionally altered pattern recognition receptors, as well as the
Hay fever 172 10.5 13 10.5
lesions themselves, could facilitate bacterial infection, resulting in
Eczema 404 24.7 38 30.7
impetiginized eczema (23,24).
There is variation in impetigo treatment guidelines (25) and no
internationally agreed standard of therapy (1). The Dutch College
Comparison with existing literature and treatment of GPs’ treatment guideline for bacterial skin infections recom-
guidelines mends avoidance of antiseptics, a maximum of 2 weeks’ initial
A Norwegian study reported incidence rates between 9 and 16 per treatment with topical fusidic acid, and 7 days of oral flucloxacil-
1000 person years in 2001 to 2004 (7), yet a 2012 study of the same lin if improvement is inadequate (26). The most recent Cochrane
population reported a much lower rate, 3 per 1000 person years (8). systematic review supports these recommendations (1). Our study
A UK study highlighted that impetigo incidence can fluctuate over found that most impetigo episodes were treated in accordance with
time, doubling or halving in a matter of years (9). the Dutch guideline. Fusidic acid, used in 85% of episodes as initial
Our study found an overall presentation incidence rate of 13.6 treatment, seemed to be satisfactory as first line agent, as only a low
per 1000 person years, with a threefold higher rate for children percentage of cases returned to the GP seeking additional treat-
under 18 years, which was comparable to other European primary ment. The proportion of oral antibiotics increased over subsequent6 Family Practice, 2018, Vol. XX, No. XX
treatments, while use of prescribed antiseptics and topical zinc was Declaration
low. Our results extend an earlier Dutch study (1987–2001) where
Funding: The study was carried out as part of our routine work and funded
there was an increase in topical antibiotic use (43% to 64%), and by departmental resources.
a decrease in use of both oral antibiotics (31% to 14%) and anti- Ethical approval: Ethical approval for the Julius General Practitioners
septics (11% to 3%) (10). Of interest was the low frequency of Network and using anonymous patient data for research purposes was given
mupirocin prescribing, despite its efficacy and popularity interna- by the Ethical Committee of the University Medical Center Utrecht, the
tionally (1). This shows the commitment of Dutch GPs to national Netherlands (Eur J Epidemiol. 2005;20:285–287).
guidelines, where mupirocin is reserved for S. aureus carriers with Conflict of interest: None.
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recurrent skin infections.
A tenth of initial treatments were with flucloxacillin, which References
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