The Laryngoscope
C 2009 The American Laryngological,
V
Rhinological and Otological Society, Inc.
Case Report
Destructive Otomastoiditis by MRSA from
Porcine Origin
Helen Van Hoecke, MD; Anne Piette, MD; Els De Leenheer, MD, PhD; Nathalie Lagasse, MD;
Marc Struelens, MD, PhD; Gerda Verschraegen, MD, PhD; Ingeboy Dhooge, MD, PhD
A 63-year-old female pig farmer was referred to
our department with a protracted course of otomastoiditis with destruction of the tympanic roof and cerebrospinal fluid leakage. The patient underwent a
cortical mastoidectomy with closure of a large dural
defect. Cultures of the middle ear effusion yielded a
methicillin-resistant Staphylococcus aureus (MRSA),
which upon further analysis was found to be from
porcine origin. To our knowledge, this is the first
report of a complicated case of otomastoiditis caused
by a pig-type MRSA.
Key
Words:
MRSA:
methicillin-resistant
Staphylococcus aureus, otomastoiditis, CSF leakage,
Staphylococcus aureus.
Laryngoscope, 119:137–140, 2009
INTRODUCTION
Since the first reports in 1961, methicillin-resistant
Staphylococcus aureus (MRSA) has become a growing
problem worldwide. MRSA strains are resistant to b-lactam antibiotics, with resistance mediated by the mecA
gene. Most MRSA isolates are also resistant to many
other antimicrobial classes.
In the United States, the proportion of Staphylococcus aureus infections due to MRSA in intensive-care
units increased from 2% in 1974 to 22% in 1995 and
64% in 2004.1
Whereas MRSA colonization or infection was initially almost exclusively confined to a nosocomial setting
(hospital-associated MRSA [HA-MRSA] and healthcareassociated MRSA), recent reports have highlighted a
From the Departments of Otorhinolaryngology (H.V.H., E.M.R.D.L.,
and Microbiology (A.P., G.V.), Ghent University Hospital, Ghent,
Belgium, and the Department of Microbiology (M.S.), Erasmus Hospital,
Free University of Brussels, Brussels, Belgium.
Editor’s Note: This Manuscript was accepted for publication September 12, 2008.
Send correspondence to Helen Van Hoecke, MD, Department of
Otorhinolaryngology, Ghent University Hospital, De Pintelaan 185, 9000
Ghent, Belgium. E-mail: [email protected]
dramatic increase in MRSA infections in individuals
without healthcare-associated risk factors (communityacquired MRSA [CA-MRSA]). CA-MRSA causes predominantly skin and soft-tissue infections (77%), followed by
wound infections (10%), urinary tract infections (4%),
and bacteremia (4%).2 CA-MRSA patients are found in a
younger age group, have fewer coexisting conditions,
and have less prior exposure to antimicrobial drugs than
patients with HA-MRSA.3
Reports on the prevalence and clinical manifestations of CA-MRSA infections in the ear are limited.
Apart from occasional reports on CA-MRSA-based infections of the outer ear canal, chronic otitis media, and a
pediatric case of acute mastoiditis, a recent study in Taiwan in 221 patients with discharging ears found a
prevalence of CA-MRSA of 12.2% or a proportion of 25%
of CA-MRSA among Staphylococcus aureus isolaties.4
During the past 10 years, MRSA has also been
increasingly reported in animals. MRSA strains found in
companion animals, such as dogs and cats, are identical
to epidemic strains found in human hospitals, indicating
that MRSA carriage in these animals is obtained from
humans. MRSA strains found in other animal species
such as horses, pigs, and cattle, on the other hand, tend
to be distinct from human strains.5 Clonal spread and
transmission of MRSA from livestock to humans in close
contact with these animals is a recent international
problem, creating a new reservoir for CA-MRSA, also
called animal-related CA-MRSA.6
We present an unusual and severe case of a complicated otitis media, caused by a community-acquired pigtype MRSA strain.
N.L., I.D.)
DOI: 10.1002/lary.20030
Laryngoscope 119: January 2009
CASE REPORT
A 63-year-old female presented at a peripheral Ear
Nose Throat (ENT) department with hearing loss and
pain in the right ear that had persisted for two months.
Review of the personal history revealed a type 2 diabetes, hypertension, and a renal cell carcinoma, treated
with partial nephrectomy two years before.
Van Hoecke et al.: Otomastoiditis by MRSA From Porcine Origin
137
softeners. The patient was treated with vancomycin intravenously until she was discharged from the hospital one
week after surgery on a further oral treatment with TMP/
SXT for three more weeks.
As potential sources of MRSA infection in this
patient, we considered the following hypotheses:
•
•
Fig. 1. CT scan shows opacification of the epitympanic space of
the right middle ear and large defect at the level of the tympanic
roof lining.
Based on otoscopic findings, ipsilateral conductive
hearing loss of 25 dB, and a flat tympanogram, the
patient was diagnosed with otitis media with effusion of
the right ear and treated with a ventilation tube.
The patient developed persistent otorrhea that was
unresponsive to treatment with local and oral ciprofloxacine and amoxicillin clavulanic acid. A CT scan of the
temporal bone showed an opacification of the right middle
ear and a large defect at the level of the tympanic roof lining (Fig. 1). Magnetic resonance imaging (MRI)
demonstrated the presence of fluid and inflammatory tissue
in the right middle ear and mastoid and confirmed the bone
destruction at the roof of the middle ear cavity (Fig. 2).
The patient was referred to our department for further investigations and treatment. b-trace protein (BTP)
in the middle ear fluid was measured by an automated
latex particle-enhanced fixed-time immunonephelometric
method on a Behring Nephelometer II analyzer (Dade
Behring, Marburg, Germany) using rabbit polyclonal
antibodies against BTP. BTP belongs to the most abundant proteins in cerebrospinal fluid (CSF). In serum and
nasal secretions, BTP is present in much lower concentrations.7 The BTP concentration in the patient’s middle
ear fluid was 41.40 mg/dl. This very high concentration
confirmed the cerebrospinal origin of the fluid.
The ventilation tube was removed in order to close
the potential route for infection. Culture of the middle
ear effusion revealed an MRSA, susceptible to trimethoprim-sulfamethoxazole (TMP/SXT), erythromycin,
clindamycin, gentamicin, and vancomycin.
After treatment with TMP/SXT, the patient underwent a cortical mastoidectomy and dural defect closure.
Extensive inflammatory tissue was removed from the mastoid and middle ear. The dura was covered with
granulomatous tissue but showed no herniation. The dural
defect was reconstructed with two onlay collagen grafts:
bicol (Codman & Shurtleff, Randolph, MA) and durasis
(Cook Biotech, West Lafayette, IN). The tegmen was closed
with bone pate. General measures to inhibit intracranial
pressure rise were applied postoperatively to assure dural
sealing: bed rest in Fowler position; avoidance of coughing,
sneezing, and nose blowing; and administration of stool
Laryngoscope 119: January 2009
138
•
MRSA obtained during a prolonged hospital stay,
including two days in the intensive-care unit, at
the time of partial nephrectomy two years before
(HA-MRSA)
MRSA acquired through direct or indirect contact
with the patient’s daughter, who worked as a
home nurse (healthcare-associated MRSA)
MRSA from porcine origin obtained at the
patient’s pig farm (animal-related CA-MRSA)
From the previous hospital stay, however, no microbiological samples were available, and the patient’s
daughter was screened MRSA-negative, leaving the ‘‘pig
hypothesis’’ to be further explored.
Preoperative samples from middle ear and mastoid
tissue were gram stained and cultured following routine
methods (5% sheep blood agar, enriched chocolate agar,
and thioglycollate, incubated for 2 to 7 days at 37 C).
Both gram stain and culture revealed no bacteria, probably due to the previous treatment with TMP/SXT.
Swabs taken from the throat, nose, and perineum of the
patient and from the nostrils of 14 pigs (one or two pigs
per pen we screened) were cultured on an MRSA ID
chromogenic (bioMérieux, Marcy l’étoile, France) agar to
detect MRSA. The patient’s nose and perineum were
MRSA-negative. The patient’s throat was positive with
an MRSA strain (same antibiogram as the middle ear
effusion). Of the 14 pigs, 10 were MRSA-positive. Four
MRSA strains (three pig origin, one patient origin) were
sent to the reference laboratory (Struelens, ULB, Hospital Erasme) for characterization by pulsed field gel
electrophoresis (PFGE) and staphylococcal protein A
(spa) typing and for detection of Panton Valentine leucocidin (PVL), a virulence factor associated with CAMRSA. They were PVL-negative, nontypeable by PFGE,
Fig. 2. Axial T2-weighted MRI shows fluid and inflammatory tissue
in the right middle ear and mastoid. Inflammatory tissue in the
mastoid contacts the dural surface.
Van Hoecke et al.: Otomastoiditis by MRSA From Porcine Origin
and belonging to spa type t011, a type frequently isolated from pigs and pig farmers.
The patient’s husband, also living on the pig farm,
was screened for MRSA carriage by sampling swabs
from the nares and throat but was found to be MRSAnegative.
The patient’s pigs were not treated for MRSA, but
protective measures including good hand hygiene and
use of dusk masks and gloves upon contact with the animals were advised.
During the weeks following surgery, the patient’s
ear pain relieved, the right middle ear became fully ventilated, and hearing recovered with a reduction in the
preoperative air-bone gap from 25 dB to 10 dB. Six
months after mastoidectomy, the patient remains well.
Upon follow-up, however, the patient’s throat remained
MRSA-positive.
DISCUSSION
A CSF leak through the middle ear only presents as
clear otorrhea when the tympanic membrane is perforated. When, however, as in the reported case, the
tympanic membrane is closed, it can be mistaken for otitis media with effusion. Fracture of the temporal bone
and skull base surgery (acoustic neuroma removal and
mastoid surgery in particular) are the most common
causes of acquired CSF leakage. Other acquired causes
of a CSF leak through the ear are chronic infectious and
neoplastic disorders of the middle ear and the mastoid.
A cholesteatoma can erode the tegmen plate and allow
herniation of dura or brain to occur over time. Congenital causes of otoliquorrhea are rare. The latter
include developmental defects of the tegmen tympani or
petrous apex with meningo-encephalocele formation and
spontaneous or posttraumatic meningeal laceration,
translabyrinthine CSF fistula—most commonly in
Mondini malformation—and casuistic reports of perilabyrinthine CSF leakage through the petromastoid canal,
facial canal, and Hyrtl’s (tympanomeningeal) fissure. In
this case, we suspected a CSF leakage because of the
pulsating watery otorrhea, persisting after placement of
a ventilation tube and unresponsive to antibiotic treatment. CSF origin of the middle ear secretion was
confirmed by the detection of b-trace, which is considered a highly sensitive and specific test. CT and MRI
were taken to localize the site of the CSF fistula and to
gain information on the underlying pathology.
It is known that infection in the tympanomastoid
space can lead to erosion of the tympanic roof, which in
turn can result in meningitis and intracranial abscess
formation. Bone erosion in chronic middle ear infections,
however, mainly occurs in the presence of cholesteatoma,
which is well known for its destructive effects on the
bone through pressure necrosis and enzymatic and
osteoclastic activity. In the absence of a cholesteatoma,
we hypothesized that the infection in the ear causing
the bone erosion that led to a cerebrospinal fluid fistula
must be caused by aggressive organisms.
Microbiologic analysis revealed MRSA from porcine
origin as the pathogen. According to a study of 50 pig
Laryngoscope 119: January 2009
farms, 68% of pig farms in Belgium are MRSA-positive
(P. Butaye, personal communication). At present the
source of MRSA in pigs is unknown, but dissemination
of MRSA among pigs is probably facilitated by the trade
of animals among different countries and the use of antibiotics for mass treatment of livestock.8 Transmission of
MRSA from pigs to people who are in close contact with
these animals, such as veterinarians and pig farmers,
creating a new zoonotic reservoir of community-acquired
MRSA, is a recently identified international problem.8,9
Cultures taken from 127 persons living on 49 Belgian
pig farms were MRSA-positive in 38% of persons. MRSA
colonization was present in 50% of persons living on a
pig farm with MRSA-positive pigs but in only 3% in
farms in absence of MRSA-positive pigs (P. Butaye, personal communication). Currently, there is no consensus
as to whether pigs should be screened and treated for
MRSA. It also remains unsure whether protective measures such as good hand hygiene and use of dusk masks
and gloves can prevent colonization upon contact with
MRSA-positive livestock. Furthermore, the possibility
that MRSA can spread airborne and can be transmitted
to animals and inviduals living in the vicinity of a pig
farm cannot be excluded.
Although MRSA transmission from animals to
humans frequently results in colonization, there are few
reports of clinical infections caused by animal-related
CA-MRSA. In Belgium, the first infection with a pigrelated MRSA strain was found in 2003 (P. Butaye, personal communication), and since then few cases were
reported. A case report of severe soft-tissue infection in
a man working on a Belgian pig farm caused by an
MRSA strain originating from a pig bite was recently
published.9 To our knowledge, however, this is the first
report worldwide of an ear infection caused by MRSA of
porcine origin. Furthermore, it is worrisome that this
strain, which does not produce virulence factors, such as
the superantigenic toxins detected in HA-MRSA or Panton Valentine leukocidin virulent factors typically
expressed by CA-MRSA strains, still managed to cause
massive bone destruction. If pig-related MRSA strains
are allowed to spread freely among pigs, from pigs to
humans and among humans, they can have a significant
impact on the epidemiology and control of MRSA. Largescale international studies are required to establish the
extent of pig-related MRSA and to determine the costeffectiveness of screening for and eradication of MRSA
in pigs and individuals in close contact with these animals. For the individual patient with severe soft-tissue
or other infection, an infection caused by MRSA has to
be considered, and special attention to anamnesis and
correct therapy should be given.
Acknowledgment
The authors acknowledge Prof. P. Butaye for invaluable information for the preparation of this article.
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