Download Skin and Soft Tissue Infections in Returning Travelers

Am. J. Trop. Med. Hyg., 80(3), 2009, pp. 431–434
Copyright © 2009 by The American Society of Tropical Medicine and Hygiene
Skin and Soft Tissue Infections in Returning Travelers
Patrick Hochedez,* Ana Canestri, Marylin Lecso, Nadia Valin, François Bricaire, and Eric Caumes
Department of Infectious and Tropical Disease, Hôpital Pitié Salpêtrière, Paris, France; Department of
Bacteriology, Hôpital Pitié Salpêtrière, Paris, France
Abstract. Skin and soft tissue infections (SSTI) are a leading cause of cutaneous problems in travelers. Sixty travelers who presented with an SSTI were prospectively included over a 20-month period. Bacterial analysis and research for
Panton-Valentine leukocidine (PVL) were performed according to clinical and bacterial presentation. The SSTI appeared
abroad in 73% and were predominantly localized on lower limbs (75%). The main clinical forms were impetigo (35%)
and cutaneous absess (23%). Insect bites were significantly associated with impetigo and ecthyma. Methicillin-susceptible
Staphylococcus aureus (MSSA) was identified in 15 patients (43%), Group A Streptococcus (GAS) in 12 patients (34%),
and an association of both in 8 (23%) among the 35 patients for whom bacteria were identified. The MSSA producing
PVL were found in 4 patients. Travelers should be advised on how to prevent arthropod exposure and susceptibility testing should be recommended considering that methicillin-resistant S. aureus (MRSA) is increasingly reported, although
not identified in our study.
was defined by a collection of pus within the dermis and
deeper skin tissues. Cellulitis referred to an acute spreading
infection of the skin that may also involve the subcutaneous
tissues. Furuncles referred to localized but deep inflammatory
necrotizing infection of the hair follicle. Folliculitis referred
to more superficial infection of the hair follicle without
necrosis.
The following epidemiologic data were recorded: age, gender, country of birth, country of residence, travel history (destination and duration), history of insect or animal bites, reason
for travel (expatriation, tourism, business travel, immigrants
returning from visiting friends and relatives in their country of origin). The time between return to France and symptom onset, and between return and presentation to our unit
was recorded, together with the following clinical signs: general health impairment, fever, lymphadenopathia, characteristic and location of the SSTI, and the presence of toe-web
intertrigo. Laboratory tests, including blood cell counts and
C-reactive protein (CRP), were only recorded in patients with
fever and/or general health impairment.
Skin samples for direct Gram staining, bacterial culture, and identification were collected from the infection
focus in all patient with impetigo, ecthyma, furuncle, and
abcess. Determination of antimicrobial susceptibility was
systematically performed, and all isolated Staphylococcus
aureus and Streptococus pyogenes strains were tested for
methicillin and erythromycin resistance. The susceptibility of
S. aureus and S. pyogenes strains was determined using the
agar diffusion method, in accordance with the guidelines of the
French Society for Microbiology.6 Specific search for PantonValentine leukocidine (PVL) was performed in S. aureus strains
when associated with necrotic and recidivant skin infection
and/or when the strains expressed an unusual resistance phenotype according to the literature.7,8 Characterization of the
genes coding for PVL (lukS-PV and lukF-PV) was performed
according to a technique described elsewhere.7 Differences
between groups were tested for significance, using the Chisquare test and the Fisher’s exact test. Data were analyzed
with SPSS software version 15.0 (SPSS, Chicago, IL).
INTRODUCTION
Skin and soft tissue infections (SSTI) cover a large spectrum
of bacterial cutaneous infections, ranging from self healing
impetigo to life threatening necrotizing cellulitis.1 The SSTI
are a leading cause of cutaneous problems in travelers during
and after return. In an international study where dermatologic
disorders were the third most common cause of health problems in 17,353 returning travelers, insect bites, with or without
super infection, skin abscess, impetigo, and erysipelas were the
first, fourth, and eleventh cause of skin diseases, respectively.2
Similarly, in two prospective studies of returning travelers with
dermatoses, SSTI, including impetigo, ecthyma, and infectious
cellulitis, were the leading skin diseases.3,4 Nonetheless, these
studies were not specifically focused on SSTI. Our objective
was to evaluate the clinical spectrum of SSTI and their bacteriologic causes in returning travelers.
PATIENTS AND METHODS
All consecutive adult travelers consulting our tropical diseases unit between January 1, 2006 and August 30, 2007 were
included if they presented with an SSTI occurring abroad or
within one month after return. Those presenting within one
month after return were included if they reported a history of
insect bites in the area of SSTI and the persistence or worsening of lesions since the day of occurrence of infection. Patients
with impetiginized scabies or marine envenomation were
excluded. Children < 15 years of age were not included, given
the absence of pediatricians in our hospital.
Travelers were defined as adults with a history of travel outside Europe. Fever was defined as a temperature of more than
38°C on admission. Within the spectrum of SSTI, we distinguished different clinical forms according to the literature.1,5
Impetigo was defined as a superficial infection of the skin
(initially vesicular, later crusted) and could be bullous or
nonbullous. Ecthyma referred to a pyoderma, which is very
similar to impetigo, but extending more deeply through the
epidermidis to produce a shallow ulcer. Cutaneous abscess
RESULTS
* Address correspondence to Patrick Hochedez, Service de Maladies
Infectieuses et Tropicales, Hôpital Pitié-Salpêtrière, 47–83 Boulevard
de l’Hôpital, 75013 Paris, France. E-mail: [email protected]
During the study period, 60 travelers (38 male, 63%) presented with an SSTI. The median age was 42 years [17–72].
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HOCHEDEZ AND OTHERS
TABLE 1
Skin and soft tissue infection (SSTI) diagnosed in 60 returning travelers and proportion of reporting insect bites
Type of SSTI number (%)
Number reporting insect bites (%)
Number of infections having
multiple locations (%)
Cutaneous abscess 14 (23%)
Ecthyma 11(18%)
Cellulitis 11 (18%)
15 (71%)
6 (43%)
8 (73%)
5 (45%)
0
12 (57%)
3 (21%)
8 (73%)
0
1 (33%)
The median length of stay abroad was 15 days [5–180]. The
median lag time between return and consultation was 7 days
[1–84]. The lesions appeared abroad in 44 cases (73%). In the
16 remaining cases, the lesions appeared after a median of
3 days [1–21] after the patient’s return. Thirty-four patients
(57%) returned from Africa, 6 (10%) from Asia, 5 (8%) from
South America, 5 (8%) from the Indian Ocean, 5 (8%) from
the Pacific, 4 (7%) from the Caribbean area, and 1 (2%)
from North America. Reasons for travel were tourism for 41
(68%), business for 11 (18%), visiting friends and relatives in
their country of origin for 6 immigrants (10%), and expatriation for 2 (3%).
The two main clinical forms of SSTI were impetigo (35%)
and cutaneous absess (23%) (Table 1). Fever was present in
9 patients (15%) and satellite lymphadenopathy was present
in 20 cases (38%). Localizations of the SSTI were as follows
(each patient could have several localizations): lower limb for
45 patients (75%), upper limb for 16 (27%), trunk for 8 (13%),
and head for 3 (5%).
Overall, 34 (57%) patients reported a history of insect bites
in the area of SSTI and 20 of them were confident about the
type of culprit insect: mosquitoes for 15 patients, spider and
flea for 2 each, and horsefly for 1 patient. When compared
with others, patients with ecthyma were significantly more
commonly reporting a history of insect bites (P = 0.044) and
presenting with multiple localizations (P < 0.001) (Table 1).
Toe-web intetrigo were observed in 3 patients (5%), 1 presenting with cellulitis and 2 with impetigo.
Bacterial identification was obtained in 35 patients (58%).
The culprit bacteria were methicillin-susceptible S. aureus
(MSSA) in 15 cases (43%), Group A β-hemolytic Streptococcus
(GAS) in 12 cases (34%), and an association of MSSA and
GAS in 8 patients (23%) (Table 2). Of the 23 MSSA strains,
1 (4%) was resistant to erythromycin and all were susceptible to pristinamycin and quinolones. Of the 21 GAS strains,
1 (5%) was resistant to erythromycin. Both GAS and MSSA
were isolated during impetigo and ecthyma (Table2), whereas
MSSA was the only bacteria isolated from cutaneous abscesses
TABLE 2
Bacterial identification according to clinical presentation
Number of bacterial isolates (%)
Type of SSTI
Impetigo
Cutaneous
abscess
Ecthyma
Cellulitis
Furuncles and
folliculitis
Furuncles and
folliculitis 3 (5%)
Impetigo 21 (35%)
Number
Number cultured (%) MSSA alone
GAS alone MSSA and GAS
21
16 (76)
5 (31)
6 (38)
5 (31)
14
11
11
8 (57)
10 (91)
0
8 (100)
1 (10)
0
0
6 (60)
0
0
3 (30)
0
3
1 (33)
1 (100)
0
0
MSSA = methicillin-susceptible Staphylococcus aureus; GAS = group A β-hemolytic
Streptococcus.
P value
0.044
< 0.001
(statistical analysis was not performed because the number of
bacterial identification was too small). Panton-Valentine leukocidine was identified in 4 patients with severe MSSA related
SSTI. One of these patients, a female with recurrent ecthyma
after a trip to Ivory Coast transmitted its strain to her male
companion who later presented with an MSSA related lower
limb cellulitis.
Blood tests were available in 14 patients: 7 had leucocytosis and 12 an increase in CRP. Outcome was favorable in all
patients, 2 patients (with infectious cellulitis) required hospitalization and 5 patients (with abscess) required surgery.
Antibiotics were prescribed in 58 (97%) patients and local
antibiotherapy in 2 (3%); oral antibiotics were prystinamycine
in 46 (77%) patients, amoxicillin in 6 (10%), and amoxicillinclavulanate in 6 (10%).
DISCUSSION
This study illustrates the broad spectrum of SSTI in returning travelers and the role of insect bites as a potential portal
of entry for these infections. In this setting, SSTI were only a
result of MSSA and/or GAS, some of these bacteria carrying
the risk of secondary transmission in the community, as illustrated in one of our cases.
The main clinical forms of SSTI (95% of cases) diagnosed
in this cohort were impetigo, cutaneous abscess, ecthyma, and
cellulitis. This spectrum looks similar to that reported in prospective studies in returning travelers where the leading skin
diseases were cutaneous abcess, impetigo, echtyma, erysipelas,
and infectious cellulitis.2–4
Bacterial identification was obtained in 58% of our patients
with positive cultures exclusively for MSSA and/or GAS. This
result can be compared with only one study in which bacterial cultures yielded S. aureus or/and GAS in 80% of the cases
of impetigo in returning travelers.3 Although widely reported
in the community in various countries and occasionally in
travelers, we did not identify a methicillin-resistant strain of
S. aureus.9–11 Meanwhile, we identified only one erythromycin resistant strain of S. pyogenes. Nevertheless, susceptibility
testing should be recommended to every traveler because the
antibiotic resistance pattern can vary according to the country
visited.1,11,12
Of the 23 patients with a staphylococcal SSTI, 4 (2 abscess,
1 ecthyma, 1 with recurrent furuncles) were infected by a
strain producing PVL. Such strains have now been clearly
associated with community-acquired severe or recurrent
necrotic SSTI, mainly furuncles, carbuncles, and cutaneous
abscesses.7,13–15 Similar to what was observed in one of our
patients returning from Ivory coast, PVL producing S. aureus
can be transmitted by close contact and carry a risk of diffusion in the community. As an illustration, two outbreaks
of severe staphylococcal cutaneous infections caused by the
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SKIN INFECTIONS IN TRAVELERS
same clone of doxycycline-resistant, PVL-positive MSSA have
been reported recently in French soldiers who had served in
Ivory Coast and who received doxycycline for malaria prophylaxis. The clone spread within families and recurrent abscesses
were reported after the soldiers’ return from Ivory Coast.16
Although our patient also presented with a recurrent ecthyma
resulting from PVL-positive MSSA after a trip to Ivory Coast,
the isolated stain was found to exhibit different bacteriologic features after polymerase chain reaction (PCR) analysis
(Croze M, Lina G, Etienne J, Vandenesch F, Center National
de Référence des Staphylocoques, Lyon, France, unpublished).
Our data and previous report of PVL-producing MSSA and
methicillin-resistant S. aureus (MRSA) in returning travelers emphasize the need for prospective studies to assess the
importance of PVL in this setting, together with management
issues and outcomes.8,10,17,18
A history of insect bite (mainly by mosquitoes) in the
affected area was reported by 57% of our travelers and was
significantly more frequently reported by patients presenting
with impetigo and ecthyma. The association between impetigo and insect bites had already been suggested in a community-based epidemiologic study conducted in England and
Wales where impetigo followed the peak of insect bites, which
peaked almost coincidentally with temperature.19
Insect bites are therefore a major cause of concern for travelers, because of the risk of malaria and arbovirus infection
but also in view of the risk of secondary bacterial infection.
With or without superinfection, insect bites were the first etiologic diagnosis in 2,947 returning travelers with a dermatologic disorder.2 Similarly, an insect bite in the affected area was
reported by 12 (63%) of 19 returning travelers with impetigo,3
and 6 (28.6%) of 21 returning travelers with infectious cellulitis.4 Nevertheless, it is still unclear whether the superinfection
is associated with scratching or whether the arthropod’s bite
or sting acts as a portal of entry.
Although toe-web intertrigo had been identified as a significant risk factor for cellulitis of the leg in studies conducted
in France (odds ratio [OR] 3.2, 95% confidence interval [CI]:
1.6–6.3) and in Tunisia (OR 5.4, 95% CI: 2.6–11.4), it was
observed in only one of our patients with cellulitis, whereas
insect bite was reported in 45% of these patients.20,21 This is
not really surprising, given that rupture of the cutaneous barrier, whatever its cause, has been shown to be a common factor associated with cellulitis in the studies conducted in France
(OR 22, 95% CI: 9.4–51.5) and in Tunisia (OR 13.6, 95% CI:
6.3–31).20,21 Other risk factors apart from toe-web intertrigo
have been associated with disruption of the cutaneous barrier
in erysipelas of the leg in Tunisia. Such factors were traumatic
wound (OR 8.8; 95% CI: 3.7–20.8%), excoriated leg dermatosis (OR 5.6, 95% CI: 1.8–17.6), and plantar squamous lesions
(OR 1.8, 95% CI: 1.1–3).21 Our results suggest that insect bites
can be added to this list.
The outcome was favorable in all patients. The main antibiotic used was pristinamycin, a streptogramin antibiotic equally
effective on GAS and S. aureus strains, including erythromycin-resistant S. aureus.22 Practice guidelines for the diagnosis
and treatment of SSTI have been recently published and are
widely applicable.1 However, some aspects need to be targeted in the setting of travel related SSTI. Travelers, at least
those with identified risks, could be recommended empiric
self-treatment in the case of some SSTI. Of note, the antibiotics to use in this setting must include agents with activity
against potentially resistant strains of both S. aureus and
S. pyogenes. Subsequently, two radically different strategies
need further evaluation. On the one hand, travelers with mild
infection could be recommended empirical self-treatment
with penicillin, oral cephalosporins, macrolides, clindamycin,
trimethoprim-sulfamethoxazole, or tetracycline.1,23 They must
be medically reevaluated in the absence of clinical response
at 24–48 hours.1 On the another hand, patients with SSTI
accompanied by signs of systemic toxicity or whose infection
is progressing despite empirical antibiotic therapy, should be
evaluated by physicians rapidly to consider immediate hospitalization, to ensure specific bacterial diagnosis procedure, and
to provide appropriate antibiotic management, assuming the
risk of community-acquired MRSA and surgical consultation
in cases of abscess and necrotizing cutaneous infections.1
Our results emphasize that travelers should be specifically
advised on how to prevent arthropod exposure, the most likely
portal of entry for SSTI in this setting. Moreover, susceptibility testing should be widely recommended considering that
MRSA is increasingly reported in various touristic countries,
although not identified in our study. Finally, the real importance of PVL-producing S. aureus in this setting needs further
prospective studies to evaluate the necessity of more specific
management.
Received June 2, 2008. Accepted for publication December 2, 2008.
Authors’ addresses: Patrick Hochedez, Ana Canestri, Nadia Valin,
François Bricaire, and Eric Caumes, Service de Maladies Infectieuses
et Tropicales, Hôpital Pitié-Salpêtrière, 47–83 Boulevard de l’Hôpital,
75013 Paris, France, Tel: 33-1-42-16-01-14, Fax: 33-1-42-16-01-65,
E-mails: [email protected], [email protected], nadia
[email protected], [email protected], and eric.caumes@
psl.aphp.fr. Maryline Lecso, Service de Bactériologie, Hôpital PitiéSalpêtrière, 47–83 Boulevard de l’Hôpital, 75013 Paris, France, Tel:
33-1-42-16-20-71, Fax: 33-1-42-16-20-72, E-mail: maryline.lecso@psl
.aphp.fr.
Reprint requests: Eric Caumes, Service de Maladies infectieuses et
tropicales, Hôpital Pitié-Salpêtrière, 47–83 Boulevard de l’Hôpital,
75013 Paris, France, E-mail: [email protected].
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