Streptococcal tonsillitis as a cause of urticaria Tonsillitis and urticaria.

Abstract

BACKGROUND: The primary role of infections in chronic urticaria (CU) is controversial. We hypothesised that streptococcal tonsillitis (ST) could be a primary cause of CU or acute recurrent urticaria (ARU). METHODS: Retrospective study of 14 outpatients observed between January 2000 and December 2009, with CU/ARU and clinical and/or laboratorial suspicion of an aetiopathogenic link with ST. Clinical history, objective examination and laboratorial study were looked for. Three groups were defined: spontaneous resolution of urticaria, resolution after tonsillectomy, and still symptomatic. RESULTS: In these patients, a causal relationship between ST and urticaria is supported by: markers of streptococcal infection, the perception of a clinical relationship between tonsillitis and urticaria, the decrease of urticaria severity with early antibiotherapy to tonsillitis and urticaria resolution after tonsillectomy. CONCLUSIONS: Our study encourages the investigation of tonsillitis in these otherwise idiopathic patients, especially until young adulthood and even in the absence of any symptoms.

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Calado
G,
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Streptococcal
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of
urticaria.
Tonsillitis
and
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ORIGINAL
ARTICLE
Streptococcal
Tonsillitis and
tonsillitis
urticaria
as
a
cause
of
urticaria
G. Calado∗, G. Loureiro,
D. Machado,
B. Tavares,
C. Ribeiro,
C. Pereira,
A.S. Luís
Immunoallergology
Department,
Coimbra
University
Hospital,
Coimbra,
Portugal
Received
9
May
2011;
accepted
24
June
2011
KEYWORDS
Angio-oedema;
Infections;
Streptococcus;
Tonsillectomy;
Tonsillitis;
Urticaria
Abstract
Background:
esised
urticaria
Methods:
ber
with
groups
still
Results: In
markers
and
urticaria
Conclusions: Our
patients,
©
The
primary
role
of
infections
in
chronic
urticaria
(CU)
is
controversial.
We
hypoth-
that
streptococcal
tonsillitis
(ST)
could
be
a
primary
cause
of
CU
or
acute
recurrent
(ARU).
Retrospective
study
of
14
outpatients
observed
between
January
2000
and
Decem-
2009,
with
CU/ARU
and
clinical
and/or
laboratorial
suspicion
of
an
aetiopathogenic
link
ST.
Clinical
history,
objective
examination
and
laboratorial
study
were
looked
for.
Three
were
defined:
spontaneous
resolution
of
urticaria,
resolution
after
tonsillectomy,
and
symptomatic.
these
patients,
a
causal
relationship
between
ST
and
urticaria
is
supported
by:
of
streptococcal
infection,
the
perception
of
a
clinical
relationship
between
tonsillitis
urticaria,
the
decrease
of
urticaria
severity
with
early
antibiotherapy
to
tonsillitis
and
resolution
after
tonsillectomy.
study
encourages
the
investigation
of
tonsillitis
in
these
otherwise
idiopathic
especially
until
young
adulthood
and
even
in
the
absence
of
any
symptoms.
2011
SEICAP.
Published
by
Elsevier
España,
S.L.
All
rights
reserved.
Introduction
Chronic
organic
The
urticaria
urticaria
(CU)
can
be
a
sign/symptom
of
a
subjacent
disease,
systemic
or
limited
to
the
skin.
causal
relationship
between
infections
and
acute
is
consensual.1Infections
are
also
well
recognised
∗Corresponding
E-mail
author.
address:
gicalado@sapo.pt
(G.
Calado).
as
CU
primary
CU
number
Mycoplasma
tuberculosis),
virus
causal
pathogenesis
unclear.2However,
an
exacerbating
factor
of
CU.2Besides
infections
and
relationship
had
been
published
as
early
as
in
1926,3a
role
of
infections
in
CU
still
controversial.
has
been
reported
to
be
associated
with
a
wide
of
infectious
agents:
bacteria
(Streptococcus
and
species,
Helicobacter
pylori,4Mycobacterium
virus
(Hepatitis
B
virus
(HBV),
Herpes
simplex
(HSV)5),
parasites6and
fungi.7,8In
some
cases,
the
relationship
was
not
proved
and
the
exact
role
and
of
mast
cell
activation
by
infections
remain
the
temporal
relationship
between
0301-0546/$
doi:10.1016/j.aller.2011.06.008
– see
front
matter
© 2011
SEICAP.
Published
by Elsevier
España,
S.L.
All
rights
reserved.

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Calado
G,
et
al.
Streptococcal
tonsillitis
as
a
cause
of
urticaria.
Tonsillitis
and
urticaria.
Immunopathol
(Madr).
2011.
doi:10.1016/j.aller.2011.06.008
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2

G.
Calado
et
al.
infections
remission
infection,
In
litis
urticaria
and
urticaria
beginning
as
well
as
urticaria
or
improvement
after
treatment
of
a
coincident
support
this
link.2
this
study,
we
hypothesized
that
streptococcal
tonsil-
(ST)
could
be
a
primary
cause
of
CU
or
acute
recurrent
(ARU).
Materials and
methods
This
in
of
and
EAACI/GA2LEN/EDF/WAO
ical
with
We
erbation
relationship
and
laboratorial
tion
differential
plement
serum
and
screening
neutrophil
auto-antibodies,
of
ova
Three
tion:
tonsillectomy
retrospective
study
included
14
outpatients
observed
the
Urticaria
and
Allergic
Skin
Disease
Consultation
our
Immunoallergy
Department,
between
January
2000
December
2009,
with
CU
or
ARU
according
to
position
paper
definition9and
clin-
and/or
laboratorial
suspicion
of
an
aetiopathogenic
link
ST.
looked
for
the
clinical
history
(symptoms,
exac-
factors
- - - namely
the
existence
of
a
temporal
between
urticaria
episodes
and
tonsillitis
- - -
clinical
evolution),
the
objective
examination
and
the
study,
including
markers
of
streptococcal
infec-
(anti-streptolysin
O
title
(ASOT))
and
other
tests:
blood
count,
renal
and
hepatic
function,
com-
fractions,
circulating
immune
complexes
(CIC),
immunoglobulins,
viral
serologies
(Hepatitis
A,
B
C
Virus,
HSV,
Cytomegalovirus
and
Epstein- - -Barr
virus),
test
for
syphilis
(VDRL),
antinuclear
and
anti-
cytoplasmic
antibodies,
thyroid
hormones
and
rheumatoid
factor,
skin
prick
tests
(SPT)
the
most
prevalent
aeroallergens
of
the
region,
stool
for
and
parasites
and
thorax
X-ray.
groups
were
defined
according
to
clinical
evolu-
spontaneous
resolution
of
urticaria,
resolution
after
and
still
symptomatic.
Results
The
of
had
lution
clinical
sented
episodes
at
that
Additionally
the
urticaria.
Some
are
The
graphical
defined
Table
14
patients
(64.3%
female)
included
have
a
current
age
25.6
±
8.3
years.
At
the
beginning
of
urticaria,
patients
17.1
±
8.0
years,
with
3.4
±
3.0
years
of
disease
evo-
until
the
first
consultation.
Relevant
data
of
the
history
and
oropharyngeal
examination
are
pre-
in
Table
1.
A
clinical
relationship
between
urticaria
and
underling
infections
was
denied
by
all
patients
the
first
consultation.
Later,
71.4%
of
patients
recognised
urticaria
exacerbations
were
coincident
with
tonsillitis.
to
anti-histamines,
antibiotic
was
prescribed
at
first
signs
of
ST,
resulting
in
less
severe
exacerbations
of
relevant
data
of
the
immunoallergological
study
presented
in
Table
1,
with
the
remaining
normal
study.
clinical
evolution
is
described
in
Table
2.
Demo-
and
clinical
differences
between
the
three
groups
according
to
clinical
evolution,
are
presented
in
3.
Discussion
An
Urticaria
prevalence
average
of
109
patients
by
year
are
observed
in
our
and
Allergic
Skin
Disease
Consultation,
with
a
of
infectious
urticaria
of
about
4.6%.10
Table
1

Relevant
data
of
the
clinical
history,
oropharyngeal
examination
and
immunoallergological
study.
Patients

Clinical
presentation
Clinical
relationship
tonsillitis/urticaria
Oropharynx

SPT

Total
IgE
(0- - -100
UI/ml)
C3

C4

C1q

C1INH

CIC

ASOT
(<200
UI/ml)
1
ARU
±
A
No
N
Negative
152

N

N
↓
N

283
2

Yes
HTC
26
N

N
↓

↑

489
3

No

167
N
N

183
4
Yes
Grasses

55
N
↑

415
5

HDM,
grasses
3500

- - -

374
6
HDM
290

- - -

224
7

No

177

- - -

711
8
Yes
Negative
427

↑

119
9

382

N

203
10

97

- - -

340
11
RA
Negative

18
↓
↑

155
12

No

HDM

27

↓

N

310
13
CU
Yes
Negative
165
N
↑

733
14

825

N

- - -

472
SPT
- - - skin
prick
test;
CIC
- - -
circulating
immune
complexes;
ASOT
- - -
anti-streptolysin
O title;
ARU
±
A - - -
acute
recurrent
urticaria
with
or
without
angioedema;
RA
- - -
recurrent
angioedema;
CU
- - - chronic
urticaria;
HTC
- - -
hypertrophic
tonsils
with
crypts;
N - - - normal;
HDM
- - -
house
dust
mites.

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Calado
G,
et
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Streptococcal
tonsillitis
as
a
cause
of
urticaria.
Tonsillitis
and
urticaria.
Immunopathol
(Madr).
2011.
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Streptococcal
tonsillitis
as
a
cause
of
urticaria

3
Table
2

Clinical
evolution
of
urticaria
and/or
angio-oedema.
Patients

Spontaneous
resolution

Tonsillectomy

Still
symptomatic

Frequency
(exacerbations/year)
of
symptoms
Time
evolution/age
of
of
disease
at
the
time
resolution
(years)
Time
evolution/age
surgery
of
disease
at
the
(years)
Time
evolution
(years)
of
disease
1

5/17

- - -

- - -

10- - -12
2

- - -

- - -

14

5- - -6
3
4

4/16
- - -
2- - -3
- - -

9
51/13

- - -

- - -

2
6

10/18

- - -

5- - -6
7

2/28

- - -

- - -

3
8

- - -

3/38

- - -
5- - -6
9

8/25

- - -
10

- - -

- - -

3

2- - -3
11

- - -

- - -

9
2
12

2/17

- - -

- - -
13 - - -8/22- - -
Daily
exacerbations/year)
(2- - -3
14

- - -

1/21

- - -
Table
3

Demographical
and
clinical
differences
between
the
three
groups
of
patients,
defined
according
to
clinical
evolution.
Spontaneous
resolution
Resolution
tonsillectomy
withStill
symptomatic
n
Female:male
Current
Age
(minimum- - -maximum,
Time
(average
Time
the
(minimum- - -maximum,
Positive
and
Clinical
5
3:2
22.4
12
(12- - -27)
1.9

5
3:2
28.6
17
(8- - -35)
3.6

4
3:1
26.0
17
(7- - -28)
5.0

age
(average
±
standard
deviation,
years)
±
5.9
±
10.7
±
8.1
at
beginning
of
symptoms;
median
(P25- - -P75)
years)
(12- - -15)
(12- - -20)
(13.8- - -20.5)
of
disease
evolution
to
the
1st
consultation
±
standard
deviation,
years)
±
1.3
±
3.3
±
3.6
of
disease
evolution
until
resolution
or
to
present;
Median
(P25- - -P75)
years)
2
(1- - -5)
(2- - -4)8
(1- - -10)
(3- - -8)9
(3- - -14)
(7.5- - -10.2)
clinical
relationship
between
tonsillitis
urticaria
1/5

5/5

4/4
presentation

4
1
RU
±
A
RA
4
1
RU
±
A
CU
3
1
RU
±
A
RA
RU - - -
recurrent
urticaria;
A - - -
angio-oedema;
CU - - -
chronic
urticaria.

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Calado
G,
et
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Streptococcal
tonsillitis
as
a
cause
of
urticaria.
Tonsillitis
and
urticaria.
Immunopathol
(Madr).
2011.
doi:10.1016/j.aller.2011.06.008
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4

G.
Calado
et
al.
In
these
14
patients,
several
were
causes
of
urticaria
allergy,
and/or
physical
thyropathy),
(parasitosis,
sinusitis
Given
coexist
our
them,
(clinical
sils
clinical
of
antibiotherapy
tonsillectomy
disease
Besides
and
literature.11In
with
respiratory
otitis,
observed
following
or
been
There
infections
the
angioedema,
of
Considering
guidelines9make
the
tious
chronic
recommended
in
ral
and
opinion,
of
since
infection.
relationship
With
ing
not
of
angio-oedema,
activation
13
by
could
high
fractions
since
of
tion
more
and

angioedema

excluded,

namely:

urticaria,
autoimmunity
(including
autoimmune
hereditary
angioedema
and
other
infections
viral
infections,
bacterial
processes
such
as
and
dental
infections).
the
high
prevalence
of
CU/ARU
and
ST,
they
can
in
the
same
patient
independently.
Nevertheless,
study
supports
an
eventual
causal
relationship
between
by
markers
of
streptococcal
infection
in
all
patients
symptoms
and/or
presence
of
hypertrophic
ton-
with
crypts
and/or
high
ASOT),
the
perception
of
a
relationship
between
tonsillitis
and
urticaria
(71.4%
patients),
the
decrease
of
urticaria
severity
with
early
to
tonsillitis
and
urticaria
resolution
after
in
the
five
patients,
with
6.0
±
3.8
years
of
evolution.
the
controversial
relationship
between
infections
CU,
namely
tonsillitis,
it
has
been
described
in
the
1967,
Buckley
et
al.
described
16
children
CU,
the
main
feature
of
15
being
recurrent
upper
infection,
pharingitis,
tonsillitis,
sinusitis
and
often
by
Streptococci
or
Staphylococci.
These
authors
that
remission
of
urticaria
was
frequently
noted
antibiotherapy.12Buss
et
al.13identified
tonsillitis
sinusitis
in
50%
of
patients
with
CU
and
high
ASOT
have
described
in
10- - -42%.2
is
a
wide
variation
in
the
reported
prevalence
of
as
a
cause
of
CU.
In
a
systematic
review
about
underlying
causes
of
physical
and
chronic
urticaria
and
eight
studies
reported
infections
in
11- - -31%
the
patients,
whereas
11
reported
them
in
0- - -6%.14
this
discrepancy,
the
EAACI/GA2LEN/EDF/WAO
no
definitive
recommendations
regarding
role
of
infections
in
urticaria,
although
testing
for
infec-
diseases
is
suggested
as
an
additional
investigation
of
spontaneous
urticaria,
and
infections
treatment
is
in
the
management
of
urticaria.11Indeed,
our
study,
the
two
patients
with
CU
reported
a
tempo-
relationship
between
CU
exacerbations
and
tonsillitis,
tonsillectomy
was
coincident
with
CU
resolution.
In
our
ST
must
always
be
looked
for,
even
in
the
absence
a
clinical
relationship
between
tonsillitis
and
urticaria,
chronic
ST
can
be
asymptomatic,
working
as
an
occult
This
fact
can
explain
the
absence
of
this
clinical
in
some
patients.
regard
to
the
aetiopathogenic
mechanism
link-
tonsillitis
and
urticaria,
a
laboratorial
pattern
was
found
in
our
study.
However,
the
laboratorial
findings
patient
2
are
similar
to
that
described
for
acquired
with
complement
consumption
through
C1q
by
CIC.
Laboratorial
data
of
patients
11
and
are
also
suggestive
of
complement
activation
mediated
CIC,
supporting
the
same
mechanism.
This
mechanism
also
be
implicated
in
those
patients
with
isolated
CIC,
admitting
that
the
normal
levels
of
complement
could
be
explained
by
the
timing
of
the
study,
not
all
patients
were
studied
during
an
active
phase
urticaria.
From
the
remaining
six
patients,
CIC
evalua-
was
not
performed
in
five
of
them.
There
is
probably
than
one
mechanism
linking
streptococcal
infection
urticaria,
which
could
be
present
alone
or
together.
Indeed,
is
A
development
discussed.
test
in
cobacter
infection
ing
result
tions
streptococcus
prevalence
population;
immune
induced
skin
these
found.
Underlying
some
of
with
for
Since
with
able.
exacerbation
was
There
not
curative
number
resolution,
tomy
clinical
would
We
experienced
relationship
by
as
We
offers
We
lectomy
consultation;
two
tion
complement
direct
activation
from
Streptococcus
described.
potential
link
between
persistent
infection
and
the
of
autoimmune
mechanisms
in
CU
has
been
In
CU,
positivity
of
autologous
serum
skin
has
been
associated
with
H.
pylori
infection
and
some
patients
this
test
becomes
negative
after
Heli-
eradication.15The
persistence
of
streptococcal
has
been
associated
with
autoreactivity,16lead-
to
rheumatic
fever
and
rheumatic
heart
disease,
which
from
autoimmune
humoral
and
cell
mediated
reac-
due
to
the
molecular
mimicry
between
haemolytic
group
A
antigens
and
host
proteins.17The
of
infections
in
CU
is
similar
to
the
general
however,
patients
with
CU
may
differ
in
their
response
to
infections,
or
may
develop
infection-
autoreactivity/autoimmunity.2Autologous
serum
test
and13C
urea
breath
test
were
not
performed
in
patients
since
a
plausible
cause
for
urticaria
was
genetic
predisposition
is
also
proposed
by
authors
as
a
possible
explanation
for
the
development
CU
in
response
to
bacterial
infection,
once
associations
major
histocompatibility
complex
II
have
been
shown
CU.18
in
these
patients
urticaria
seems
to
be
associated
ST,
its
early
treatment
and
frequency
decrease
is
desir-
As
referred
before,
prompt
antibiotherapy
improved
severity
but
the
long-term
clinical
evolution
discrepant
between
patients
(Table
2).
are
well
defined
criteria
to
tonsillectomy
that
do
include
this
one
alone.19In
our
study,
tonsillectomy
was
in
the
five
patients.
However,
given
this
restricted
and
the
fact
that
some
experienced
spontaneous
we
cannot
assess
the
effectiveness
of
tonsillec-
in
order
to
recommend
it
to
all
patients
with
this
picture.
Probably,
there
are
prognostic
factors
that
be
important
to
find
out.
observed
that
patients
with
spontaneous
resolution
a
shorter
time
of
disease
evolution.
A
clinical
between
tonsillitis
and
urticaria
was
reported
all
patients
who
did
not
have
spontaneous
resolution,
opposed
to
1/5
in
the
group
of
spontaneous
resolution.
can
speculate
that
the
longer
time
of
disease
evolution
more
opportunities
to
perceive
this
relationship.
propose
that
those
patients
who
accomplish
tonsil-
criteria
should
be
promptly
referenced
to
an
ENT
the
others
should
be
followed
during
the
first
years
of
disease
evolution
and
if
a
spontaneous
resolu-
does
not
occur,
tonsillectomy
should
be
considered.
Conclusion
Although
increasing
may
roborates
Our
as
activation,
given
randomised
controlled
trials
are
lacking,
there
is
evidence
that
recurrent
or
persistent
infections
have
a
primary
role
in
CU
or
ARU.
Our
study
also
cor-
this
relationship,
at
least
in
some
patients.
laboratorial
data
suggest
complement
activation
the
main
immunopathogenical
mechanism
of
mastocyte
besides
the
pathogenesis
of
CU
or
ARU
in
any
patient
may
be
multifactorial.

Page 5

Please
Allergol
cite
this
article
in
press
as:
Calado
G,
et
al.
Streptococcal
tonsillitis
as
a
cause
of
urticaria.
Tonsillitis
and
urticaria.
Immunopathol
(Madr).
2011.
doi:10.1016/j.aller.2011.06.008
ARTICLE IN PRESS
+Model
ALLER-334;

No.
of
Pages
5
Streptococcal
tonsillitis
as
a
cause
of
urticaria

5
The
prognosis
of
urticaria
is
favourable
when
the
aetiol-
ogy
identification
ever
tonsillitis
until
toms.
Larger
tors
patients
is
established.
Therefore,
it
should
be
treated
by
the
and
elimination
of
underlying
causes
when-
possible.
Our
study
encourages
the
investigation
of
in
these
otherwise
idiopathic
patients,
especially
young
adulthood,
and
even
in
the
absence
of
any
symp-
studies
are
warranted
to
define
prognostic
fac-
of
longstanding
disease
in
order
to
better
select
those
who
would
benefit
from
tonsillectomy.
Conflict
of interest
The
authors
have
no
conflict
of
interest
to
declare.
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