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Journal of Infection (2016) xx, 1e7

www.elsevierhealth.com/journals/jinf

Impetigo and scabies e Disease burden


and modern treatment strategies
Daniel K. Yeoh a, Asha C. Bowen a,b, Jonathan R. Carapetis a,b,*

a
Princess Margaret Hospital for Children, Perth, Western Australia, Australia
b
Telethon Kids Institute, University of Western Australia, Perth, Western Australia, Australia
Available online - - -

KEYWORDS Summary Impetigo and scabies both present different challenges in resource-limited
Scabies; compared with industrialised settings. Severe complications of these skin infections are com-
Skin sores; mon in resource-limited settings, where the burden of disease is highest. The microbiology,
Impetigo; risk factors for disease, diagnostic approaches and availability and suitability of therapies also
Pyoderma; vary according to setting. Taking this into account we aim to summarise recent data on the
Children; epidemiology of impetigo and scabies and describe the current evidence around approaches
Paediatrics to individual and community based treatment.
ª 2016 Published by Elsevier Ltd on behalf of The British Infection Association.

Introduction Impetigo

Both impetigo and scabies are common infections of the Background


skin with a large global burden.1,2 In the industrialised
world, significant complications from impetigo and scabies Impetigo is a common superficial skin infection which
are rare whilst in resource-poor settings and certain mar- predominantly affects young children.3,4 It is estimated
ginalised communities, their collective impact is much that more than 162 million children are suffering from
greater. There are several effective options for the treat- impetigo at any one time.2 The burden of disease is highest
ment of both impetigo and scabies. Despite this, challenges in low-income countries and within marginalised popula-
remain in addressing the burden of disease on a community tions in developed nations.2 Infection is caused by invasion
level in regions where infection is endemic. of the epidermis by bacteria colonising the skin following

* Corresponding author. Telethon Kids Institute, University of Western Australia, West Perth, Western Australia 6872, Australia.
Tel.: þ61 894897777.
E-mail addresses: daniel.yeoh@health.wa.gov.au (D.K. Yeoh), Asha.Bowen@menzies.edu.au (A.C. Bowen), Jonathan.Carapetis@
telethonkids.org.au (J.R. Carapetis).

http://dx.doi.org/10.1016/j.jinf.2016.04.024
0163-4453/ª 2016 Published by Elsevier Ltd on behalf of The British Infection Association.

Please cite this article in press as: Yeoh DK, et al., Impetigo and scabies e Disease burden and modern treatment strategies, J Infect
(2016), http://dx.doi.org/10.1016/j.jinf.2016.04.024
2 D.K. Yeoh et al.

minor trauma. Autoinoculation is common and the infection are not always available in resource-limited settings and
is highly transmissible. Hot and humid climatic conditions, treatment of typical cases without microbiology is
poor access to water and possibly overcrowding are factors empiric.22 Nonetheless, in the current milieu of increasing
which play a role in frequent impetigo transmission in antimicrobial resistance,6 regional data on causative bacte-
endemic areas.4 riological agents and their antibiotic sensitivity profiles
The bacterial aetiology of impetigo varies according to remain vital to best direct empiric therapy and to monitor
region and continues to change over time. In tropical for changing patterns of resistance.4
climates Streptococcus pyogenes (Group A Streptococcus
or GAS) remains the major pathogen3,4 and co-infection Treatment
with Staphylococcus aureus is common.5 In temperate cli-
mates S. aureus has largely replaced S. pyogenes as the
When determining impetigo treatment, there are several
predominant pathogen in impetigo6 and community ac-
important factors including the extent of disease, commu-
quired methicillin resistant S. aureus (CA-MRSA) is of
nity wide prevalence, likely adherence to treatment and
increasing importance worldwide.6e8
known antimicrobial resistance. Most of the clinical trials
for impetigo treatment relate to limited or uncomplicated
impetigo, defined as fewer than 5 lesions. Where, impetigo
Clinical manifestation, complications and diagnosis
is extensive (greater than 5 lesions) or community preva-
lence is high, refer to the treatment section on extensive
Impetigo can present as bullous lesions or non-bullous,
impetigo.
papular lesions that go on to form a crust. Bullous impetigo
is caused by S. aureus whilst non-bullous lesions are associ-
ated with both S. pyogenes and S. aureus as described Limited or uncomplicated impetigo
above. Ecthyma is a deep form of impetigo in which ulcer- A Cochrane systematic review concluded that topical
ation extends into the dermis. In the developed world antibiotics are the most effective treatment for limited
impetigo is a common reason for presentations to primary impetigo.23 This review included 68 randomised control tri-
health care providers but it is generally a self-limiting con- als representing 5578 participants,23 finding that mupiro-
dition in this setting.9 In resource-limited settings severe cin, fusidic acid and retapamulin were all superior to
disease and complications of impetigo remain placebo and there was no difference demonstrated be-
problematic3,4,10 tween the most commonly studied topical agents: mupiro-
Invasive infections such as erysipelas (involving the cin and fusidic acid. In addition, there was no significant
dermis and lymphatics), cellulitis (involving subcutaneous difference found in 7-day cure rates between topical and
tissue), osteomyelitis, septic arthritis and bacteraemia can oral antibiotics (excluding erythromycin which is inferior
all complicate impetigo. S. pyogenes bacteraemia and to topical mupirocin) and topical antibiotic use was associ-
streptococcal toxic shock syndrome are commonly pre- ated with fewer adverse events.23 The review also cited a
ceded by skin and soft tissue infection.11,12 S. aureus bac- lack of supportive evidence for the use of disinfectant solu-
teraemia carries a high mortality and skin infection is an tions in the treatment of impetigo.23
important risk factor in settings where impetigo is There are several factors to consider when selecting a
common.8,13 topical antibiotic. Resistance to mupirocin and fusidic acid
Where S. pyogenes is the predominant pathogen, impe- among S. aureus isolates is increasing in association with
tigo can also lead to significant immune-mediated compli- increased use of these agents.6,24 Although retapamulin
cations. In endemic settings most cases of acute post- has demonstrated good in vitro activity against methicillin
streptococcal glomerulonephritis (APSGN) are preceded by resistant S. aureus (MRSA), its efficacy in clinical trials
impetigo.14,15 Individuals with a history of APSGN in child- against MRSA infections has been variable25,26 and it is
hood are at increased risk of developing ongoing albumin- not approved for the treatment of MRSA infections. More-
uria and chronic kidney disease in later life.16,17 There is over, S. aureus isolates with elevated minimum inhibitory
also a plausible link between S. pyogenes skin infection concentrations (MICs) to retapamulin have been described,
and acute rheumatic fever.18 This hypothesis is supported although the clinical significance of this is uncertain.27
by the presence of very high rates of rheumatic fever and There are calls to restrict the use of topical fusidic acid
rheumatic heart disease in Aboriginal populations in in order to preserve the oral formulation as a useful agent,
Australia wherein impetigo is pervasive and S. pyogenes in combination with rifampicin, for difficult-to-treat MRSA
throat infection is uncommon.19 infections.24 Topical fusidic acid is not available for use in
The diagnosis of impetigo is generally made clinically. the USA and this is reflected in the Infectious Diseases Soci-
The use of clinical algorithms may aid in the identification ety of America (IDSA) guidelines for skin and soft tissue
and treatment of impetigo in resource-limited settings. For infection which recommend topical retapamulin or mupiro-
example, the WHO Integrated Management of Childhood cin for uncomplicated impetigo.22
Illness (IMCI) skin algorithm has been assessed in Fiji and
demonstrated improvement in the clinical recognition of Extensive impetigo
impetigo.20 Elsewhere, flipcharts using high quality photo- Determining the optimal treatment of extensive impetigo,
graphs and clinical descriptions are used to train health particularly in resource-limited settings where the burden
care workers in diagnosing impetigo.21 Gram stain and cul- of disease is highest, remains a challenge.4 It is generally
ture of skin swabs to confirm the aetiological agent are accepted that the use of systemic antibiotics for extensive
often recommended22 but adequate laboratory resources disease is practical and appropriate, yet there are limited

Please cite this article in press as: Yeoh DK, et al., Impetigo and scabies e Disease burden and modern treatment strategies, J Infect
(2016), http://dx.doi.org/10.1016/j.jinf.2016.04.024
Impetigo and scabies 3

data comparing therapies for this indication4,23 and this is a Bacterial decolonisation may play a role in the manage-
clear limitation of the Cochrane review on treatment of ment of patients with recurrent skin infections, the pre-
impetigo.23 Furthermore the demonstrated frequency of vention of post-surgical infections and in hospital based
co-infection of S. pyogenes with S. aureus and the emer- MRSA control,22,34,35 however the utility of decolonisation
gence of CA-MRSA present additional challenges in selecting in the prevention of impetigo on a community level is un-
appropriate therapy.5,6 Antibiotic treatment of affected in- clear. Recent randomised controlled trials in military co-
dividuals leads to resolution of impetigo lesions which likely horts assessing nasal mupirocin36 and topical
reduces transmission. Studies to date have not explored the chlorhexidine37 respectively failed to demonstrate any
effect of antibiotics on rarer endpoints such as invasive reduction in S. aureus skin and soft tissue infections. In
infection or APSGN due to the large sample size required. addition to the practical issues of implementing ongoing
Further work is needed to understand the full benefits of topical decolonisation measures on a community level,
treatment of extensive impetigo, and the potential risk of the widespread community use of mupirocin and/or chlor-
inducing more widespread antimicrobial resistance if anti- hexidine could result in the increased circulation of S.
biotics are widely dispensed in highly-endemic aureus strains resistant to these agents and thus limit their
communities. effectiveness.27,38,39 Recommendations for the use of
The available systemic treatment options for impetigo chemoprophylaxis to decolonise household contacts of
have some limitations. Benzathine penicillin G (BPG) has cases of invasive S. pyogenes disease vary and clear evi-
been widely used however it is poorly accepted in some dence of efficacy in preventing invasive disease is lack-
settings due to its intramuscular (IM) route of administra- ing.12,40 The role of broader community based S.
tion and its efficacy has been questioned with the emer- pyogenes decolonisation in the prevention of skin disease
gence of S. aureus as a pathogen in impetigo.4 Empiric has not been assessed.
therapy with S. aureus cover is recommended for extensive It is clear that the greatest burden of impetigo and its
impetigo however oxacillins and first generation cephalo- complications is borne by resource-limited populations,
sporins lack activity against MRSA and may not be appro- where it is critical to focus on disease prevention. There
priate in settings where methicillin-resistance is is ongoing work in the development of a vaccine against
common.22 Amongst oral agents with activity against GAS which could offer a cost-effective and practical avenue
MRSA, tetracyclines are contraindicated for use in children for disease prevention, although a vaccine is not immi-
and liquid formulations of lincosamides are unpalatable for nent.41 In the interim, advocacy to improve access to
this age group. Co-trimoxazole (TMPeSMX) is an attractive health services, sanitation and housing and to reduce over-
option in that it is cheap, licenced for use in children and crowding in areas where impetigo is highly prevalent should
is available in a palatable liquid formulation. Although be a major focus in disease prevention. There is some evi-
the conventional wisdom is that TMPeSMX lacks activity dence that greater access to swimming pools42,43 and a
against S. pyogenes there are both in vitro25 and in vivo28 combination of hand-washing and daily bathing44 can
data to challenge this perception.29 reduce the burden of impetigo. On a broader scale, as evi-
A recent large clinical trial demonstrated non-inferiority denced in the industrialisation of Asian countries such as
of oral co-trimoxazole compared to IM BPG in the treatment Singapore, complications such as APSGN can be virtually
of impetigo in Indigenous children in Northern Australia.10 eliminated in the setting of improved socioeconomic status,
The majority of participants (72%) had extensive disease housing and health services.45
and S. pyogenes and S. aureus were isolated from 90%
and 81% of participants respectively. Clearance of S. pyo-
genes (but not S. aureus) was associated with clinical reso-
Scabies
lution of sores, highlighting the primary role of S. pyogenes
in impetigo pathogenesis in this setting.10 The only other Background
study that has clear findings for this context compared
oral amoxicillin with oral erythromycin for treatment of Scabies is an infection of the skin caused by the mite Sar-
impetigo. Treatment success was achieved in 89% of both coptes scabiei var hominis. The adult mites burrow into
groups, although microbiology was not available.30 Presum- the epidermis and reproduce. In the epidermis, the mites
ably the high success rate seen in this study was also due to and their excreta produce a delayed hypersensitivity reac-
the dominance of S. pyogenes in the microbiology of tion which is responsible for the rash and pruritus associ-
impetigo. ated with scabies infestation. Transmission is
predominantly via prolonged skin-to-skin contact and
Community treatment and prevention most commonly occurs between members of a household.46
Community based drug administration in certain scenarios Unsurprisingly scabies infection is associated with over-
may reduce the burden of disease associated with impetigo crowding and socioeconomic disadvantage4,46,47 and chil-
particularly in the setting of APSGN outbreaks and in dren carry the highest burden of disease.48 The
communities where scabies infestation is widespread. A prevalence of scabies was found to range from 0.2% to
review of observational studies of such outbreaks in North- 71.4% in a recent systematic review of population based
ern Australia concluded that targeted treatment of children studies.48 The highest prevalence is seen in tropical re-
with skin sores and household contacts of cases using BPG gions, such as Central America, the Pacific islands and
was warranted.31 In communities where scabies is endemic, Northern Australia.48 In developed countries prevalence is
targeted or mass community treatment of scabies has also generally low but outbreaks amongst populations in institu-
been shown to reduce the prevalence of impetigo.32,33 tionalised care are well described.47

Please cite this article in press as: Yeoh DK, et al., Impetigo and scabies e Disease burden and modern treatment strategies, J Infect
(2016), http://dx.doi.org/10.1016/j.jinf.2016.04.024
4 D.K. Yeoh et al.

Clinical manifestations, complications and application of topical scabies therapies can result in skin re-
diagnosis actions and tolerability may be further reduced in humid
tropical climates.49
During primary infection, the appearance of symptoms is Ivermectin is an oral scabicide which was previously
delayed until 4 weeks following initial contact.46 Patients reserved for cases of scabies refractory to topical therapy
present with a papular or vesicular eruption which is but is increasingly seen as a useful agent for both individual
intensely pruritic, usually worse at night. The mites are and community based treatment.55 As ivermectin is not
most often found in web spaces of the fingers, on the ovicidal a second dose is recommended 8e15 days following
wrists, in the axillae, around the umbilicus and in the groin the initial dose to prevent recrudescence.47 The efficacy of
or the popliteal fossa. Other family members may also have oral ivermectin is superior to placebo and topical lindane
pruritus. The distribution of infestation is different in in- whilst trials comparing oral ivermectin to topical benzyl
fants with involvement of the palms, soles and scalp.49 benzoate have demonstrated mixed results.49,54 In the Co-
Scabies infestation is associated with significant compli- chrane review of scabies therapies, topical permethrin
cations related to secondary infection with bacteria. Bac- was found to be superior to oral ivermectin although the
terial infection, particularly with S. pyogenes and S. length of follow up in included trials ranged from 1 to 2
aureus, is a well-recognised complication of scabies infes- weeks only.49
tation.1,4,5,13 The presence of scabies is associated with Although ivermectin is an effective and well-tolerated
complications of impetigo including invasive bacterial agent in the treatment of scabies there remain some
infection and post-streptococcal glomerulonephritis.11,13,14 limitations to its use. Resistance is a potential concern
As discussed earlier, in endemic settings the treatment of particularly in endemic communities.56 Also, there are
scabies at a community level has been shown to reduce limited data demonstrating safety and tolerability of iver-
the prevalence and severity of skin sores32 and mectin in infants57 and it is not yet licensed for the treat-
haematuria.33 ment of uncomplicated scabies in many regions.
Crusted scabies is a severe form of scabies where the
host immune system fails to control the number of mites.50 Community treatment and prevention
It is characterised by crusted, hyperkeratotic lesions with The treatment of the close contacts of patients with
mite numbers reaching millions in some patients.50 Cases scabies is recommended in order to prevent re-infection
classically occur in immunosuppressed patients and those and further transmission although there is a lack of data
in institutional care although, in particular communities, supporting this strategy.55 Topical permethrin is considered
patients with no underlying risk factors are also affected.50 first-line therapy,47 however poor compliance amongst con-
Because of the high mite burden, contacts of patients with tacts has been identified as a barrier to the efficacy of this
crusted scabies are at high risk of infestation themselves51 approach.58 Oral ivermectin is an alternative agent for the
and this may drive community outbreaks. treatment of contacts which may prove effective and more
Diagnosis of scabies is predominantly based on the acceptable than topical therapies but this has yet to be as-
clinical findings of intense pruritus and a typical distribu- sessed in comparative trials.46,47 There is a clear need for
tion of papules. Skin scrapings occasionally reveal mites, further research in this area with a recent Cochrane review
ova or faeces, however microscopy is time consuming, of failing to identify any well-designed randomised trials as-
low-yield and may be impractical in resource-limited sessing prophylactic measures to prevent the transmission
settings.46,52 While dermatoscopy is a potentially useful of scabies.59
diagnostic tool, the cost of equipment and the reliance Mass drug administration (MDA) may be an alternative
on appropriate training are limitations.52,53 As with impe- approach to scabies control in settings where scabies is
tigo, clinical algorithms designed for use in resource- endemic.46,55 This strategy has been explored as a control
limited settings have shown promise in increasing case measure using permethrin60,62 and ivermectin33,61,62
identification and warrant further evaluation.20 Certainly respectively with promising results. Notably, a recently
comparison between studies examining prevalence and published randomised trial assessing the effectiveness of
treatment outcomes is hindered by the lack of consensus scabies MDA in Fiji compared ivermectin MDA and
criteria for the diagnosis of scabies.48,49 Further research permethrin MDA with standard care (i.e. permethrin
in designing simple and accurate diagnostic tests for scabies treatment of cases and contacts) in three separate island
is ongoing. communities.62 There was a significant and sustained
reduction in scabies and impetigo in all three groups with
the most marked effect in the ivermectin group followed
Treatment by the permethrin MDA group.62 A significant reduction in
the community prevalence of scabies has previously been
Individual treatment demonstrated following the implementation of an iver-
There are various topical therapies utilised in the treat- mectin MDA program for the treatment of lymphatic filari-
ment of scabies. In a Cochrane review of randomised asis in Tanzania.63 This study highlights the potential for
control trials comparing scabies therapies, permethrin collaborative research in assessing the effects of MDA pro-
was found to be the most effective topical therapy (supe- grammes on a number of neglected tropical diseases
rior to lindane and crotamiton).49 Benzyl benzoate is including scabies.64
another effective topical therapy that is preferred in As with impetigo, the long-term control of scabies in
some resource-limited settings due to the relatively high endemic settings is greatly dependent on addressing the
cost of permethrin, but is less well tolerated.46,54 The social determinants of health within these populations.

Please cite this article in press as: Yeoh DK, et al., Impetigo and scabies e Disease burden and modern treatment strategies, J Infect
(2016), http://dx.doi.org/10.1016/j.jinf.2016.04.024
Impetigo and scabies 5

Crusted scabies treatment 6. Bangert S, Levy M, Hebert AA. Bacterial resistance and impe-
It is recommended that patients with crusted scabies be tigo treatment trends: a review. Pediatr Dermatol 2012;
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gressive increase in community-associated methicillin-resis-
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scabies. With regards to community control, active case 8. Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler Jr VG.
identification and treatment of core transmitters with Staphylococcus aureus infections: epidemiology, pathophysi-
crusted scabies within a population is a potential adjuvant ology, clinical manifestations, and management. Clin Micro-
approach in endemic settings.51 biol Rev 2015;28(3):603e61.
9. Koning S, Mohammedamin RS, van der Wouden JC, van Suijle-
kom-Smit LW, Schellevis FG, Thomas S. Impetigo: incidence
Conclusions and treatment in Dutch general practice in 1987 and 2001 e
results from two national surveys. Br J Dermatol 2006;
The significant impact of scabies and impetigo on the 154(2):239e43.
health of people in resource-limited settings has in the 10. Bowen AC, Tong SY, Andrews RM, O’Meara IM, McDonald MI,
past been under-recognised. Promisingly, there is growing Chatfield MD, et al. Short-course oral co-trimoxazole versus
interest and advocacy concerning scabies and skin sores as intramuscular benzathine benzylpenicillin for impetigo in a
demonstrated by the recent formation of the International highly endemic region: an open-label, randomised, controlled,
non-inferiority trial. Lancet 2014;384(9960):2132e40.
Alliance for the Control of Scabies55 and the inclusion of
11. Gear RJ, Carter JC, Carapetis JR, Baird R, Davis JS. Changes in
scabies on the WHO list of neglected tropical diseases in
the clinical and epidemiological features of group A strepto-
2013. There is advocacy for impetigo to be included on coccal bacteraemia in Australia’s Northern Territory. Trop
this list as well.2 Med Int Health TM IH 2015;20(1):40e7.
There are safe and efficacious treatments available for 12. Boyd R, Patel M, Currie BJ, Holt DC, Harris T, Krause V. High
these common skin infections, yet in many areas where burden of invasive group A streptococcal disease in the North-
disease burden is highest, little has changed with regards to ern Territory of Australia. Epidemiol Infect 2016;144(5):
control. Ongoing research exploring risk factors and aeti- 1018e27.
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both individual and community based treatment is tigation of a cluster of Staphylococcus aureus invasive infec-
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14. Currie BJ, Carapetis JR. Skin infections and infestations in
rates of skin disease in certain communities is of chief Aboriginal communities in northern Australia. Australas J Der-
importance. Whilst in the industrialised world scabies and matol 2000;41(3):139e43. quiz 44e5.
impetigo are often considered trivial, ongoing efforts to 15. Marshall CS, Cheng AC, Markey PG, Towers RJ, Richardson LJ,
address the major impact of these infections in the Fagan PK, et al. Acute post-streptococcal glomerulonephritis
developing world remain extremely important. in the Northern Territory of Australia: a review of 16 years
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Conflict of interest
16. Hoy WE, White AV, Tipiloura B, Singh G, Sharma SK,
Bloomfield H, et al. The multideterminant model of renal dis-
The authors have no conflict of interest to declare. ease in a remote Australian Aboriginal population in the
context of early life risk factors: lower birth weight, child-
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(2016), http://dx.doi.org/10.1016/j.jinf.2016.04.024
6 D.K. Yeoh et al.

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Please cite this article in press as: Yeoh DK, et al., Impetigo and scabies e Disease burden and modern treatment strategies, J Infect
(2016), http://dx.doi.org/10.1016/j.jinf.2016.04.024