Journal of Hospital Infection (2007) 67, 264e270

www.elsevierhealth.com/journals/jhin

Outbreak of staphylococcal bullous impetigo in a maternity ward linked to an asymptomatic healthcare worker
P. Occelli a, M. Blanie b, R. Sanchez b, D. Vigier b, O. Dauwalder c, A. Darwiche b, B. Provenzano b, C. Dumartin a, P. Parneix a, A.G. Venier a,*
Centre de Coordination de la Lutte contre les Infections Nosocomiales du Sud-Ouest, CHU, Bordeaux cedex, France b rigueux, Pe rigueux cedex, France Centre hospitalier de Pe c fe rence des Staphylocoques, Faculte Laennec, INSERM U851, Centre National de re Lyon 1, France Universite
Received 23 May 2007; accepted 31 August 2007 Available online 18 October 2007
a

KEYWORDS
Staphylococcal scalded skin syndrome; Bullous impetigo; Pemphigus neonatorum; Outbreak; Neonate; Nosocomial; Chronic carriage; Healthcare worker

Summary An outbreak of staphylococcal bullous impetigo occurred over a period of ve months in a maternity ward involving seven infected and two colonised neonates. The skin lesions were due to epidermolytic toxin A-producing Staphylococcus aureus. Infection control measures were implemented and a retrospective casee control study performed. Contact with an auxiliary nurse was the only risk factor for cases of bullous impetigo (P < 0.01). The nurse cared for all seven cases and was an asymptomatic nasal carrier of the epidemic strain. Repeated courses of decontamination treatment failed to eradicate carriage. Nine months after the last case, another neonate developed a more severe form of bullous impetigo and the auxiliary nurse was reassigned to an adult ward. 2007 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved.

Introduction
* Corresponding author. Address: Centre de Coordination de la Lutte contre les Infections Nosocomiales du Sud-Ouest, CHU, 33076 Bordeaux cedex, France. Tel.: 33 55 679 6058; fax: 33 55 679 6012. E-mail address: anne-gaelle.venier@chu-bordeaux.fr

Staphylococcal skin infections are among the commonest skin diseases in children.1 Bullous impetigo, also known as pemphigus neonatorum, and the

0195-6701/$ - see front matter 2007 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jhin.2007.08.023

Bullous impetigo outbreak staphylococcal scalded-skin syndrome (SSSS) represent a collection of blistering skin diseases induced by epidermolytic toxins A (ETA) and B (ETB).1,2 Whereas in bullous impetigo the toxin produces blisters locally at the site of infection, in SSSS it produces blisters at distant sites.1 SSSS remains a potentially fatal condition particularly in its generalised form, with a mortality rate <5% among children.1,2 Many outbreaks of bullous impetigo and SSSS have been reported among neonates.3e10 Risk factors for staphylococcal outbreaks include carriers in close contact with infants, improper cord hygiene, overcrowding, understafng and inadequate infection control practices.2e6,9e12 We describe here an outbreak of seven cases of staphylococcal bullous impetigo in a maternity ward.

265 2. Audits of hand hygiene and equipment cleaning were carried out. 3. Antibiotic cream (fusidic acid) and topical antiseptic (chlorhexidine) were applied on the skin lesions, twice a day until the disappearance of the lesions (7e10 days). Two infected neonates received systemic antibiotics (cloxacillin or a combination of oxacillin and aminoglycoside) for seven days. Once a fth case was diagnosed at the end of August, further control measures were implemented: 4. Each staff member underwent S. aureus nasal screening. 5. From 1 September, every neonate underwent S. aureus nasal screening three days after birth. 6. Environmental sampling of surfaces in the operating suite and in delivery rooms, and surfaces and common equipment in the neonatal intensive care unit (ICU) were carried out. In the postpartum unit, baby bathtubs, midwives trolleys, infant care trolleys, balances and tap water were sampled. In bedrooms, baby crib, swaddling table, sink, and mothers bed were sampled. 7. Cleaning protocols were reviewed and each housekeeper was dedicated to an area. 8. Gynaecological surgery was temporarily ceased until the strain source was discovered, since operating theatres and staff were shared with the obstetric unit. 9. The outbreak was notied to the SouthWestern France Infection Control Coordination Centre and to the Departmental Health Authority. 10. Parents and general practitioners of colonised neonates were informed about the risks and asked to notify any skin lesions to the maternity unit.

Methods
Hospital setting
The hospital of Perigueux is a 1325-bed public hospital in South-Western France. The maternity unit has 44 beds with an obstetric unit performing about 1000 deliveries per year. It employs 64 healthcare workers (HCWs).

Recognition of an outbreak
In May 2005, the laboratory microbiologist noticed Staphylococcus aureus from swabs of skin lesions from two neonates. As the occurrence of two similar cases appeared unusual, he alerted the infection control team and a follow-up of new cases began. A third case appeared in June so infection control measures were implemented. A fourth neonate was infected in mid-July. The strains from the third and fourth cases were sent to the French National Staphylococcal Reference Centre, which revealed that they were the same ETAproducing S. aureus strain.

Epidemiological study
A retrospective and cross-sectional caseecontrol study was performed to determine the risk factors of this outbreak. An outbreak case was dened as a neonate, born in the maternity unit between 14 May and 14 September 2005, who developed bullous impetigo and from whom cultures of the lesions produced ETA-producing S. aureus. A potential case was dened as a neonate, born in the maternity unit in the same period who developed bullous impetigo but had not been cultured or was negative. A colonised neonate was dened as a neonate, born in the

Infection control measures

Once the outbreak was identied, the following infection control measures were implemented: 1. The infection control team reminded staff about standard and complementary precautions (hand washing, barrier precautions, isolation measures, and environmental cleaning). Posters were displayed in the unit and a staff meeting was organised.

266 maternity unit in the same period, who screened positive for ETA-producing S. aureus but did not develop bullous impetigo. A control was dened as a neonate, born in the maternity unit in the same period, who did not develop bullous impetigo and, if screened, was negative for S. aureus. Neonates with skin lesions caused by other S. aureus strains were excluded. Each case was matched with two controls, randomly chosen within the neonates born in the same week in the maternity unit. Colonised neonates were excluded. The infection control team collected information on cases and controls from medical reports using a standardised questionnaire. Characteristics of neonates (sex, birth weight, term of delivery, length of stay in the hospital, underlying diseases, carriage of invasive device, ICU stay) and of their skin lesions (presence, delay from birth until the appearance of the blisters, localisation, treatment performed, date and result of lesion swabbing) were collected. The date of hospitalisation of their mothers and the characteristics of the delivery (vaginal or caesarean birth, labour duration, premature rupture of membranes, obstetrical manoeuvres, septicaemia or skin lesions) were also collected. HCWs in charge of mothers and neonates during and after delivery, and who performed the neonates rst care, were identied. A plan of the unit was used to locate the rooms occupied by the neonates.

P. Occelli et al.

Molecular methods
S. aureus isolates were tested for toxin production at the French National Staphylococcal Reference Centre. Gene sequences encoding staphylococcal toxins (TSST-1, SEA, SEB, SEC, SED, SEH, SEK, SEL, SEM and SEO) and ETA and ETB were detected by using polymerase chain reaction-based methods.13

Results
The outbreak took place over ve months. Two potential cases and two outbreak cases appeared between 14 May and 6 July 2005. One outbreak case appeared in August. They were all infected by an erythromycinekanamycin-resistant S. aureus strain. In September, 86 neonates were screened. Eighteen (20.9%) were nasal carriers of S. aureus, of whom four carried the epidemic strain. Two of the latter developed bullous impetigo in September making a total of seven cases. All cases were apyrexial. The blisters were located mainly on the face but also on neck, arm, buttock and axillary exure. Skin lesions appeared on average ve days after birth (three to six days). All cases resolved after treatment. One neonate, negative on screening, was rehospitalised seven days after birth for bullous impetigo. A different S. aureus strain was isolated. The occurrence of seven cases over ve months suggested an intermittent source of infection with no overlapping period between cases or colonised neonates. The geographical distribution of cases in the unit did not suggest a spatial cluster. Babies and mothers were together in private rooms distributed between the two oors of the ward. Only one room was successively occupied by two cases: case 4 (July 2005) and case 5 (August 2005). All the environmental samples were negative except in the room occupied by cases 4 and 5, where the baby bed and bath were contaminated. This room was closed and thoroughly cleaned. It was only used again after negative control samples. Staff audits did not show any major failure in hygiene practices, with hand hygiene, environmental disinfection and umbilical care all being adequately performed. The records of one control showed that he suffered from skin lesions. As the mother had identical lesions at the time of the delivery, it was assumed that the baby was infected by her strain and no sample was taken. He was excluded from the caseecontrol study and the seven cases were then compared with 13 controls (Table I). Hospital stay was from three to 11 days for cases

Statistical analysis
The association between explanatory variables and the presence or absence of infection, was rst tested by univariate analysis. The association with quantitative variables was tested with Manne Whitney U-test. The association with qualitative variables was tested with Fishers exact test. Only variables with P < 0.20 were integrated in an exact multivariate logistic regression. Software LogXact was used.

Microbiological methods
Environmental samples, swabs from skin lesions and noses were routinely cultured using selective agar plates (bioMe rieux, Marcy lEtoile France). Antibiotic susceptibility of S. aureus isolates was determined using the automated system Vitek 2 (bioMe rieux). Erythromycin and kanamycin resistance was the antibio-phenotype used for presumptive identication of the outbreak strain.

Bullous impetigo outbreak

Table I Characteristics of the cases, the controls and their mothers Case (N 7) Neonates Sex ratio (M/F) Average stay at hospital (days), mean (SE) Average birth weight (g), mean (SE) Mothers Average labour duration (h), mean (SE) Premature rupture of membrane, N/total (%) Caesarean, N/total (%) Obstetrical manoeuvres, N/total (%) Mothers dermatological lesions, N/total (%) Contact with healthcare workersa Contact with the colonised auxiliary nurse, N (%)
a

267

Control (N 13) 0.5 5 (1) 3275 (332) 7 1/11 3/13 1/12 1/14 (6) (9) (23) (8) (7)

P-value 0.4 0.9 0.7 0.7 0.9 0.6 0.5 0.3 <0.01

0.7 6 (3) 3346 (552) 6 1/6 2/7 1/5 0/7 (2) (17) (29) (20) (0)

7 (100)

3 (23)

The association with other healthcare workers was not signicant (data not shown here).

and three to seven days for controls. Investigation showed that an auxiliary nurse had been in contact with all seven cases. The caseecontrol study identied contact with this auxiliary nurse as the only signicant risk factor for bullous impetigo. Of the 64 HCWs in the maternity ward, 15 (23.4%) were S. aureus nasal carriers. The auxiliary nurse carried the epidemic ETA-producing S. aureus. She worked in the delivery area and demonstrated good hygiene practices. She was removed from duty until she completed a topical treatment (nasal mupirocin for ve days and daily shower with povidone iodine for three days). Her husband, a HCW in the same hospital, was also found to carry the epidemic strain and received the same treatment. They were advised to reinforce home cleaning and both returned to work after negative swabs. The main results of the genotype analysis of S. aureus strains from cases, HCWs and the environment are presented in Table II. By the end of September 2005, as the auxiliary nurse was negative, environmental reservoirs were eliminated and no other cases occurred. Nasal screening of neonates was stopped and gynaecological surgery was recommenced. The two HCWs were regularly screened, as recommended.14 In October 2005, the auxiliary nurse became positive again and decontaminated (mupirocin and povidone iodine showers). She was negative in January 2006 but positive in February. Screening was stopped, as she appeared to be a chronic carrier. She was asked to follow precautionary hygiene practices such as mask wearing and the use of alcohol-based solution (on nonsoiled hands) before and after handling babies. In June 2006, an eighth neonate developed severe skin lesions due to the epidemic ETA-producing

S. aureus. He was treated with systemic antibiotics and infection control measures were implemented. He had been in contact with the auxiliary nurse. A nasal swab conrmed she was still a carrier. She was removed from duty while she and her husband completed a topical treatment (mupirocin) and an eight-day course of systemic treatment (sulfamethoxazole and trimethoprim). After discussions between the auxiliary nurse, the infection control team, the board of directors, maternity ward management and occupational health, she was moved to an adult ward. After her reassignment, no further cases of bullous impetigo occurred.

Discussion
Over 13 months, eight cases and two colonised neonates were affected by the same strain of S. aureus. The investigation and case-control study identied an asymptomatic HCW carrying and transmitting the epidemic strain to neonates. It is known that HCWs have a higher prevalence of S. aureus carriage than the general population in which carriage rate is already around 30%.2,7 Outbreaks of ET-producing S. aureus due to HCWs have been reported in maternity wards. They originated from infected carriers (chronic otitis and paronychia) or from asymptomatic carriers frequently suffering from chronic skin diseases (psoriasis, cutaneous T-cell lymphoma, atopic or contact dermatitis).2e6,9,11,15 Our carrier suffered neither from an infection nor from a chronic skin disease. She may well have acquired the strain from infants at her previous work in a child-care centre or from her husband who works in an emergency room.

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P. Occelli et al.

Table II Pulsotype and genotype of staphylococcal strains from infected and colonised neonates, healthcare workers and environment Strain origin Infected neonatesa Colonised neonates Healthcare workers Auxiliary nurse Pulsotype agr allele Toxin genes sea seb sec sed see seh sek sel sem seo tst eta etb etd lukS-PV lukF-PV lukD-lukE lukM Edin hlB hlg hlg2 mecA gene
a

Environment Bed Bath

Auxiliary nurses husband A 2

A 2

B 4

A 2

A 2

C 2 e

A 2

A 2

A 2

The strains of the rst and the second cases of the outbreak were not sent for genotyping.

Colonised HCWs may initiate outbreaks of ETproducing S. aureus but they can also be initiated by colonised mothers passing their strain onto their own baby, which is then a source for acquisition and further transmission by HCWs.2,10,16 Mothers were not screened during the investigation as the epidemic curve favoured an intermittent source of transmission rather than cross-transmission and all cases mothers were asymptomatic. It was decided to screen the staff rst and mothers would have been screened if no source had been found. Although appropriately performed, the decolonisation procedure failed to eliminate S. aureus nasal carriage from the auxiliary nurse. A previous study showed that 60% of treated HCWs were again carriers (of the same strain or a new one) one year after the treatment.17 Carriage relapse could also have been due to intrafamilial transmission between the auxiliary nurse and her husband or from contamination of their home environment.18,19 Cases of refractory S. aureus carriage in nurses have been

described in relation with the contamination of soft-furnishing (beddings, carpet, clothing), furniture (chairs, door handles and computers) and domestic pets. Cleaning of hand-touch sites and soft furnishings, along with daily laundry of clothes and topical clearance therapy for all the family can be successful. In our case, the two staff members did not have a pet, and home cleaning was advised, but no subsequent investigation was performed to assess the level of contamination. It was originally decided to keep the auxiliary nurse on duty in the maternity ward because cases were clinically benign and she co-operated with hygiene measures. The occurrence of a more severe case in June 2006 underlined the difculty of continuing high-level hygiene measures in the long term. In particular, permanent mask-wearing was probably given low priority as it is uncomfortable and can stigmatise the carrier. Bertin et al. described a similar situation linked to a S. aureus chronic carrier nurse.15

Bullous impetigo outbreak SSSS can occur in adults with high mortality rates in the case of underlying diseases.1,2 Thus, wards with immunocompromised patients were excluded for our carriers reassignment. Her relocation was made possible only because she allowed her medical record to be made available and her chronic carriage status declared to the board of directors. This situation highlighted the lack of guidelines regarding HCWs as chronic carriers of epidemic strains when caring for vulnerable patients. Some neonates were colonised by the epidemic strain having had no contact with the carrier. They were probably contaminated by cross-transmission through HCWs hands or contaminated objects.20 Inanimate objects such as baby baths, ophthalmoscopes, stethoscopes, otoscopes, laundry carts, air ducts and magazines can harbour S. aureus and be a source for cross-transmission.2,6,20 This episode reafrms that hygiene procedures in general and hand hygiene in particular constitute the rst barrier to prevent such outbreaks. During the investigation, other S. aureus strains were identied among neonates. The presence of circulating strains in maternity wards has already been highlighted in other studies.3,6,7,10,21 Genotyping studies remain useful for investigations in order to distinguish epidemic strains from circulating strains. This study revealed seven cases, but other neonates may have developed the infection when back home. We think that severe cases would have been re-hospitalised, but some benign cases might not have been notied. From 1998 to 2000, the French National Staphylococcal Reference Centre received 113 notications of staphylococcal toxaemia in children. Thirty-four cases were bullous impetigo and ETA was the most frequent toxin found.22 In France, staphylococcal toxaemia notication is not compulsory and exhaustive epidemiological data is not available. Therefore the number of cases among children and the occurrence of outbreaks may be underestimated. Our study showed that a caseecontrol format is an efcient and easy complementary method of investigation. Although only two controls per case were studied, it conrmed the auxiliary nurse as the source of the outbreak. Dancer et al. also used a retrospective analysis to conrm three asymptomatic nurses as the source of an outbreak of pemphigus neonatorum in a maternity unit.9 As in our situation, the outbreak ended after the carriers had been treated. We had fewer cases (seven versus 80) probably because our carrier was unique and had particularly good hygiene practices. Difculties in nding carriers can explain why the two

269 outbreaks took place over few months. In Perigueux, earlier detection could have shortened the course of the outbreak. In conclusion, this outbreak was due to a chronic carrier among the staff and was only temporarily stopped by the reinforcement of infection control measures. There are difculties in maintaining specic high-level hygiene measures in the long term, and the management of such a situation remains difcult.

Acknowledgements
We thank the healthcare workers involved in this outbreak for their active co-operation. Conict of interest statement None declared. Funding sources None.

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