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Journal of Clinical Microbiology, February 2001, p. 728-729, Vol. 39, No. 2
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.2.728-729.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Breast Milk Transmission of a Panton-Valentine
Leukocidin-Producing Staphylococcus aureus Strain Causing
Infantile Pneumonia
Isabelle
Le Thomas,1
Patricia
Mariani-Kurkdjian,1
Anne
Collignon,2
Alain
Gravet,3
Olivier
Clermont,1
Naïma
Brahimi,1
Joël
Gaudelus,4
Yannick
Aujard,5
Jean
Navarro,6
François
Beaufils,7 and
Edouard
Bingen1,*
Service de
Microbiologie,1 Service de
Néonatologie,5 Service de
Gastro-Entérologie,6 and Service
de Réanimation,7 Hôpital
Robert Debré, Paris, Service de
Microbiologie2 and Service de
Pédiatrie Générale,4
Hôpital Jean -Verdier, Bondy, and Institut de
Bactériologie de la Faculté de Médecine,
Strasbourg,3 France
Received 5 September 2000/Returned for modification 17 October
2000/Accepted 31 October 2000
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ABSTRACT |
We report on a 38-day-old infant who developed pleuropneumonia due
to a Staphylococcus aureus strain responsible for familial furunculosis, which was acquired by maternal breast-feeding. All isolates from the infant and parents were genetically related by
randomly amplified polymorphic DNA analysis and produced
Panton-Valentine leukocidin.
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TEXT |
Staphylococcal pleuropneumonia in
infants and children is a public health problem in developing countries
but has become rare in industrialized countries. Severe respiratory
disease in immunocompetent children and chronic furunculosis have been
associated with Staphylococcus aureus strains that produce
Panton-Valentine leukocidin (PVL), a cytotoxin that causes leukocyte
destruction and tissue necrosis (4, 8).
Case report.
We report on a 38-day-old infant who developed
pleuropneumonia due to a PVL-producing S. aureus strain
responsible for familial furunculosis, which was acquired by maternal
breast-feeding. This breast-fed infant, born at 40 weeks of gestation,
was admitted to the neonatal unit of Robert Debré Hospital with
septic shock. She had developed retroseptal periobital cellulitis
following conjunctivitis and ethmoiditis diagnosed by contrast-enhanced axial computed tomography of the orbit.
She was leukopenic (leukocyte count, 2,500/mm3; 87%
neutrophils) and febrile (temperature, 39°C) and had a marked
inflammatory syndrome (C-reactive protein level, 361 mg/liter;
fibrinogen level, 6.7 g/liter). Antimicrobial therapy was started with
cefotaxime (100 mg/kg of body weight/day) plus fosfomycin (200 mg/kg/day). Eye pus (sample S1), a sample from a cheek wound (sample
S2), and, subsequently, a sample for blood culture (sample S3) yielded S. aureus. The mother's breast milk (sample S4), sampled
after local disinfection, also yielded S. aureus. On day 3 after onset, the initial antimicrobial regimen was replaced by
oxacillin (200 mg/kg/day) and gentamicin (5 mg/kg/day) plus rifampin
(20 mg/kg/day) on the basis of susceptibility testing and in vitro
time-kill curve studies. The infant subsequently developed respiratory
failure and was admitted to the intensive care unit for bilateral
staphylococcal pneumonia. On days 5 and 6 of illness, two samples for
blood cultures (samples S5 and S6) were positive for S. aureus. Blood cultures became sterile 4 days after the beginning
of second-line treatment. The chest X-ray film showed infiltrates,
pneumothorax, and pleural extravasation, which required chest tube
drainage. Samples of the draining pleural fluid were sterile.
Respiratory function improved very slowly, and the production of
compressive bubbles on the mediastinum led, 5 months later, to partial
resection of the lower right lobe.
Surveillance cultures were performed because of the chronic
furunculosis in both parents. Samples from the father's nostrils
(sample S7) and throat (sample S8) and the mother's groin (sample
S9)
yielded
S. aureus.
Identification of
S. aureus was based on colony morphology,
coagulation of citrated rabbit plasma (bioMérieux, Marcy
l'Etoile,
France), and production of a clumping factor
(Staphyslide test;
bioMérieux).
A total of seven isolates from the neonate (isolates from samples S1,
S2, S3) and the parents (isolates from samples S4, S7,
S8, and S9) were
genotyped and analyzed for PVL production. Randomly
amplified
polymorphic DNA (RAPD) analysis with two primers (primer
A3
[5'-AGTCAGCCAC-3'] and primer 217
2
[5'-GCCCCCAGGGGCACAGT-3'])
was used for genotyping,
as described previously (
1). Unrelated
isolates of
S. aureus obtained from two patients hospitalized
in two
different wards of our hospital were studied for comparison.
The seven
isolates from the infant and parents were genetically
related to each
other and were unrelated to the control strains
(Fig.
1), confirming both the origin of the
septicemia in the
infant and the intrafamilial transmission. PVL
production was
characterized by using a previously described PCR method
(
8).
As expected, a fragment of 433 bp was obtained with
the seven
isolates (Fig.
2). PVL
production was confirmed by immunoprecipitation
assay (H. Monteil,
Institut de Bactériologie de la Faculté de
Médecine,
Strasbourg, France).
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FIG. 1.
DNA fingerprinting of S. aureus by RAPD
analysis with primer A3 (5'-AGTCAGCCAC-3') Lane  ,
bacteriophage molecular size marker; lanes 1 to 7, isolates from
samples S1, S2, S3, S4, S7, S8, and S9, respectively; lanes 8 and 9, unrelated isolates.
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FIG. 2.
PCR detection of the PVL gene. Lane , bacteriophage
molecular size marker; lanes 1 to 7, isolates from samples S1, S2,
S3, S4, S7, S8, and S9, respectively; lanes 8 and 9, negative
controls.
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Discussion.
The incidence of orbital infection secondary to
ethmoiditis in children increases with age and is rare before age 1 year (10). We describe a 38-day-old infant who developed
pleuropneumonia preceded by periorbital infection with a PVL-producing
strain of S. aureus that was transmitted by maternal
breast-feeding.
Leukocidin is a two-component toxin which targets polymorphonuclear
cells, monocytes, and macrophages (
11). Its toxicity
involves two unlinked exoproteins (class S and class F components)
which lead to transmembrane pore formation and ultimately to cell
death. PVL induces a process of necrosis by stimulating granulocyte
synthesis of inflammatory mediators. PVL also participates in
the
extension of the infection by inhibiting phagocyte functions
and
provoking destruction of these granulocytes (
7). This may
have been responsible for the marked leukopenia in our
patient.
PVL production can lead to secondary organ involvement, especially of
the lungs. In this infant the initial infection (of
the ethmoid sinus)
may thus have been propagated via septic metastasis
to the lungs,
leading to pleuropneumonia with marked necrosis
of the pulmonary
parenchyma and major functional sequelae. PVL
has been found in 85% of
S. aureus strains isolated from patients
with
community-acquired pneumonia (
8). Pneumonia due to
PVL-producing
S. aureus has been associated with septicemia
(
3). Early appropriate
antibiotic treatment is thus
crucial (
2). Blood cultures became
sterile only after 4 days of a second-line antibiotic regimen
(oxacillin and rifampin plus
gentamicin). Similar late responses
to treatment have been described
previously (
3) and have been
linked to the number and size
of pulmonary abscesses, which hinder
eradication of the pathogen. PVL
has been found in 86% (
9)
and 93% (
8) of
S. aureus strains isolated from furuncles. Both
of the
infant's parents had chronic furunculosis. In the patient
presented
here, familial carriage of the strain was probably responsible
for
transmission to the infant during breast-feeding. Familial
carriage of
S. aureus has been shown to be a risk factor for subsequent
infection with the same organism in neonates (
6).
Recurrent
furunculosis and small familial outbreaks of furuncles are
difficult
to treat (
5). Strict hygiene measures and
decolonization of
parents with chronic furunculosis due to
PVL-producing
S. aureus strains, and particularly
breast-feeding mothers, might reduce
the risk of
transmission.
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FOOTNOTES |
*
Corresponding author. Mailing address: Service de
Microbiologie, Hôpital R. Debré, 48, Bd. Sérurier,
75019 Paris, France. Phone: 33 (1) 40 03 23 40. Fax: 33 (1) 40 03 24 50. E-mail: edouard.bingen{at}rdb.ap-hop-paris.fr.
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Journal of Clinical Microbiology, February 2001, p. 728-729, Vol. 39, No. 2
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.2.728-729.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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