Chronic Inflammation
Is Associated
with
an Increased Proportion of Goblet Cells
Recovered
by Bronchial Lavage*
John
R.
Spurzem,
David
M.
Stephen
To
tify
M.S.PH.;
MS.;
I. Rennard,
M.D.
evaluate
could
M.D.,
Daughton,
the
provide
changes
,
possibility
sufficient
cell
for
bronchial
cells,
hum,
later
cells,
easily
trifugation
and
James
a process
Epithelial
cells,
with
to quan-
T
epithelial
asymptomatic
cent,
he
with
cells
(chronic
22
findings
muscle
by
chronic
airway
wall fibrosis
is easily identified
and
that
smokers
peripheral
mal
is increased
airways
to enrich
including
ciliated
Giemsa
subjects.9
smokers
patients
with
the relationships
airway
abnormality,
possible
to
serially
between
and
evaluate
evaluating
Assessment
autopsy
of
material
within
degree
same
lung..”
*From
the
Critical
Rennard;
ofPathologv
Medical
Manuscript
Reprint
lungs.
Center,
Medicine
Daughton;
in the
in nor-
changes
been
the
has
wide
variation
between
of
multiple
Internal
Medicine,
Section
(Drs.
Spurzem,
and Ms. Mueller),
and
Microbiology(Dr.
might
be
investigators
are consisin the
of the
bronchoscopic
Linder),
University
Pulmonary
analysis,
cells
BAL
p<O.O5),
Thus,
bronchoalveolar
derived
inflammation
in
(r
the
first
bronchial
percent
lavage
epithelial
in the spectrum
important
specimens
pathologic
1991;
100:389-93)
might
be inadequate
for reproducibly
Evaluation
expectorated
enough
cells
the method
sputum
has
been
shown
to
for evaluation
ofcell
differentials,’2’3
requires
plugs
of sputum
free
abnormalities.
and may be
composition
Bronchoalveolar
lavage
lower
later
(20
ml)
(BAL)
BAL
airway
yield
means
cells.’”
By
aliquots
can
The
varia-
is an effective
tract
first-infused
19
of
provide
but
of oral
hampered
by wide
within
sputum
respiratory
aliquots,
in assessing
for
of columnar
underlying
pathologic
small
is
cells
quantifying
contamination
bility in cellular
0.72,
infused
lavage
fluid
technique
We
pro-
separately
enriched
has
inflammation.
choscopy
and
chronic
BAL
were
bronchitis
for
been
useful
hypothesized
in 28 patients
airflow
obstruction
comparison,
in 15 smokers
and 33 normal,
nonsmoking
without
chronic
volunteers.
suggest
adequate
that
BAL
hi-
chial
epithelial
bronchitis
with
and
increased
provides
recovery
of goblet
with
and,
for
bronchitis
The results
samples
cells for evaluation
airflow
obstruction
of bron-
and that chronic
is associated
with
cells.
METHODS
of Nebraska
13.
Medical
performed
with
Thompson,
and
the Department
Center,
Omaha.
received
October
9; revision
accepted
December
requests:
Dr
Spurzem,
Pulmonary
Section,
VA
600 South
42nd
Street,
Omaha
68198-2465
of airflow
and
the
FEy
bronchoalveolar
seen
reflect
Significorrelated
a visually
(Chest
=
opsy
measures
airway
changes.
I
and
index,
sufficient
may
strongly
neutrophils
and the changes
epithelial
ANOVA).
was
that BAL with separation
of the first infused
aliquots
would
be useful
in quantifying
changes
in epithelial
cell numbers
associated
with chronic
bronchitis.
Bron-
required
is seen
percent
bronchial
in
bronchitis
of
of providing
from
specimens
bronchioles
of bronchitis
as the
the
cessing
difficulties
Smaller
such
p<O.00l,
percentage
measures
of sampling
interventions,
have not been
with a bronchoscope
except
that several
pathologic
changes
even
in
shown
features.
abnormality
Department
and
of
histologic
airway
abnormality
Care
Mr.
and
cells
seen
have
or excised
Thus,
A feature
bronchitis
function.6’9”#{176} However,
because
a bronchiole,
of
hypertrophy,
pathologic
therapeutic
lung function
airway
such as those
obtained
considered
assessable
have noted
that while
tent
lung
are
smooth
of goblet
with those
bronchitis
reduced
with
bronchitis
cell
at bronchoscopy
capable
36 ± 2 per-
compared
gland
and
with
other
score
(9 ± 1 percent,
goblet
aliquots
(r0.44,
(r
0.74,
p<O.00l).
stain.
metaplasia,
and inflammation.
in patients
with
Anatomic
and
to correlate
of chronic
numbers
compared
the
p<O.00l),
bronchitics
submucosal
subjects
cantly,
known
2 percent)
cell
normal
with
of desquamated
epithepreparation
by cytocen-
±
goblet
hypertrophy,
and
obstruction
a modified
smokers
pathologic
characterized
F.C.C.P;
M.D.;
cells obtained
in
were
processed
Qu antification
of the columnar
cell types
revealed
that
those
with chronic
bronchitis
and asymptomatic
smokers
have
increased
goblet
cells as a percentage
of the total
columnar
M.D.,
tinder,
lavage
cells
associated
types
the epithelial
aliquots
that
and fragments
identified
after
staining
Thompson,
bronchoalveolar
epithelial
aliquots,
contents.
goblet
were
B.
PA.;
F.C.C.P
that
in epithelial
from
Mueller,
respiratory
inflammation,
we examined
the first
infused
(20
ml)
separately
Austin
Mary
The
with
airway
study
population
a history
obstruction,
was
of cigarette
composed
smoking
15 subjects
with
CHEST
Downloaded From: http://journal.publications.chestnet.org/pdfaccess.ashx?url=/data/journals/chest/21631/ on 06/18/2017
of three
and
a history
I 100
groups:
chronic
I 2 1
28 subjects
bronchitis
ofcigarette
AUGUST,
and
smoking,
1991
389
hut
without
airway
cough,
sputum
obstruction,
were
and
selected
met
for
inclusion
the following
the
month
years;
for
at least
with
to seek
medical
FEV,
less
this
than
for
one
fixed
airway
diseases
been
than
exacerbation
patients
without
chronic
smoking
at least
two
85
normal
volunteers
in the
six weeks
preceding
was
Protection
and
were
normal
To obtain
were
used
into
those
of Knudson
by
assigning
abnormal)
for each
by
lobe
BAL
was
The
aliquot
first
pooled and
site.
to
solution,
Each
lobes.
time.
performed
saline
mon-
airways,’9
aliquots
independent
the
and
a scale
the
results
that grades
The
normal,
and
airway
observers
lingula;
secretions.n
site,
from
prepared
cells
and
and roentgenographic
t#{149}
20-mI
index
3
for
was
severely
summing
aliquots
into
aspirated
each
separately
samples
with
five
temperature,
immediately
from
processed
Bronchial
l)e enriched
was
instilling
room
the
the
in this
proteins
:
evidence
the
was
used.
t tests
with
used.
and
Park,
for
Shandon
cells.
The
cells
Giemsa
stain
IL). To more
stained
by
were
prepared
Wright
with
readily
a mucicarmine
by cotinting
Epithelial
The
To
SEM
±
three
the
200
cells
were
cells
in
examined
whether
existed,
differences
analysis
of
determine
differences
between
Bonferroni
adjustment
for
between
index,
correlation
To detect
.
groups
correlations
bronchitis
The clinical
been described
and
Briefly,
two
in all six sites
at
as mean
of
ing medical
predicted
bronchoscopy
and
(0 to 3; 0
by
cells
100,000
determined
FEV,
cell
and
age
specific
multiple
counts
were
variance
and
tests
smoking
calculated
using
coefficient.
RESU
ered
than
of three
to minimize
bronchial
final
of sterile
four
manner
thought
suggests
dwell
samples,
aliquots
have
were
at each
been
found
to arise
from
that
the earliest
the
attention
in
of the
patients
tended
Epithelial
stains.
(Fig
from
three
to have
subjects
numbers
The
more
were
easily
typically
(6. 1
(3.6
identified
Wright-Giemsa
Columnar
1). Three
chronic
cells
recov-
2.2 X 10)
0.6 x 10)
±
±
examination.
cells
modified
bronchoscopy
(3.7 ± 0.5 x 10), but all groups
ofcells
in the bronchial
sample
cell
major
types
had
or
were
categories
identified:
ciliated
columnar
ciliated
but had degenerated
called
“ciliocytophthoria,”E
cells
the
groups.
in the bronchial
sample
lavage
did the asymptomatic
smokers
for cytologic
the
resulted
any
normal
adequate
had
LTS
characteristics
of the three
groups
have
previously.2#{176} No complications
requir-
or the
all the
each
BAL
bronchitis
scores.
normal
were
reported
Spearman’s
and coworkers.2i
index,’
a score
characteristic
The
described.’
were quantitated
using a ‘bronchitis
erythema,
edema,
friability,
and
determined
histor,
Board
for carbon
standards.
for analysis,
assessed
each
and
of
also
preparations.
means
groups,
PA)
were
sample
(Cytospin;
McGaw
samples
followed
solution
a modified
Scientific,
cells,
After
mesh
preparations.
are
among
bronchial
salt
with
to the
Review
capacity
to ATS
visually
aspi-
descrihed.’
nylon
cytocentrifugation
stained
differentials
same
Data
were
Subjects.
previously
Cell
the
Sewickle;
and
cytocentrifugation
had
infection
according
Institutional
cells
until
study.
diffusing
by examining
smokers
airways
previously
balanced
by
American
(ANOVA)
were
and
tract
all subjects
according
as
BAL
the
from
Research
performed
study
respiratory
of Nebraska
were
of the
an
smoking
if they
asymptomatic
entry
epithelial
was
to
time
The
obtained
bronchial
inflammation
at the
only
the
through
mm),
Hanks’
dried
goblet
on the
had
8
Instruments,
air
stain.
lung
The
in
as
filtration
(400g.
Southern
were
the
Further-
study
included
an tipper
single-breath
performed
values
day
if the
had
within
processed
by
examination
identify
of albuterol,
subject
the
were
had
of Human
Spirometry
prior
not
of the University
for the
BAL
per
of predicted.
had
consent
guidelines
oxide
packs
percent
of entering
bronchitis
selected
eosinophils.
centrifugation
(Diff-Quik;
minimize
of inflammatory
or if the
(3)
in
excluded
inhalation
evidence
bronchitis,
six weeks
were
after
or more
for
chronic
within
a FEV
5 percent
To
substantially
were
of mucus
resuspended
and
were
remain
fluids
removal
cytologic
included
bronchitis
subjects
two
subject
years;
subjects
described.
or more
excluded
two
The
chronic
Thus,
contained
other
Informed
with
obstruction.
were
previous
previously
subjects
by 15 percent
subjects
of the
BAL
of
dyspnea
the
aliqtiots
ration.u
days
previous
led
lavage
if they
most
the
which
of predicted.
have
group
as increased
ofsputum,
or
Subjects
on
during
defined
in each
sputum
more,
a year
attention,
the
bronchitis
and sputum
exacerbation,
76 percent
improved
if the
01’
months
in quality
variables,
FEV,
six
smokers),
volunteers.
chronic
(1) cough
a change
investigation
clinical
(asymptomatic
nonsmoking
in the
criteria:
(2) at least
associated
production
33 normal,
using
the
either
mucicarmine
clearly
identifiable
of columnar
cells
were
cells, cells that had been
and lost visible
cilia (also
and goblet
cells. Ciliated
a columnar
shape
with
an
obvious
4
..
:4
..
p
FIGURE
and
ciliated
390
air
1 . Columnar
epithelial
cells. Aliquots
ofbronchial
sample
cells were prepared
drying
prior
to staining
with a modified
Wright-Giemsa
stain (Diff-Quik).
cells (C) are readily
identified
(original
magnification
x 400).
Chronic
Inflammation
by cytocentrifugation
Goblet
cells
(C)
Associated
Downloaded From: http://journal.publications.chestnet.org/pdfaccess.ashx?url=/data/journals/chest/21631/ on 06/18/2017
and
with Goblet
Cells
(Spurzem
at a!)
end
plate
was
also
and
cilia.
A spectrum
with
the cilia
seen
absent.
However,
typical
cation
the
morphologic
as a ciliated
identified
by their
the
modified
stain
was
of degenerating
partially
removed
presence
of the
features
type
end
40
cells
or
plate
and
S
usually
allowed
identificell.
Goblet
cells
were
different
morphologic
Wright-Giemsa
features
stain.
The
30
a,
c
with
mucicarmine
20
used
in an attempt
mucus-containing
mine
goblet
stain
and
was
cellular
not
cells.
specific
debris
mucicarmine
to specifically
stain
However,
in that
were
not
the
some
also
did
stain
C
0
S
mucicar-
S
S
S
Thus,
.
any
S
S
C
0
macrophages
stained
provide
the
the
S
#{149}5
55
S
S
10
S
S
particular
S
55
55
5
S
S
advantage
over
determining
Fragments
were
and
modified
noted
epithelium
reserve
joined
attempt
these
changes
recovered,
also
cells
monolayer.
We
of goblet
cells
two observers
was
(r
=
good
0.81).
icantly
were
be
spectrum
been
can
be
did
not
of epithelial
our attention
counted
The
(Fig
and
ciliated
cells
each
counting
100
interobserver
different
evaluated
10
20
FIGURE
3.
30
cells
Correlation
bronchitis
expressed
bronchitis
40
as a percent
between
index
for all three
as a percentage
index.
50
60
of total
columnar
goblet
subject
of the
cell
70
80
cells
proportions
and
the
groups.
Ordinate:
goblet
cells
total
columnar
cells;
abscissa:
changes.
in the
we focused
could
.
.5.’.
Goblet
on the
single
columnar
cells.
These
cells could
be easily
grouped
into ciliated
cells (including
those
degenerated
cells
in which
the cilia were
partially
gone
or lost) and
goblet
(secretory)
cells. Thus,
columnar
epithelial
cell
differentials
S
*
seen
as has
Metaplastic
to quantify
S..
.
squamous
hyperplasia
in a cohesive
To quantify
were
hyperplasia,
cell
described.24’
loosely
in
stain
0
to demonstrate
and
previously
Wright-Giemsa
_1&
cell types.
of bronchial
metaplasia,
cells
the
2). The
were
proportions
of goblet
when
the
(p<0.001
determined
columnar
correlation
proportions
in
cells
by
cells.
There
the
counts
were
signif-
means
of the three
groups
, ANOVA).
Furthermore,
101
when
the
compared
of goblet
group
means
of
between
cells was
compared
and
the
goblet
cell
with
asymptomatic
proportion
was
elevated
compared
with
normal
smokers
proportions
the specific
groups,
the
elevated
in the chronic
smokers
in the
and
neutrophils
cells,
we
with
both
the
percentage
cells.
The
to
determine
was
associated
subjects
compared
the
if the
(p<O.Ol).
the
changes
percentage
of
in the
cells)
goblet
bronchitis
of goblet
epithelial
of airway
in columnar
percentages
derived
of neutrophils
of columnar
epithelial
cells
airway
inflam-
presence
with
visually
(p<O.Ol)
asymptomatic
To correlate
the changes
in columnar
with other
measures
of bronchitis
and
mation
were
proportion
bronchitis
cells
bronchial
(as
correlated
cells
index
and
lavage
a percentage
with
the
bron-
‘I)
a)
5,
0
a,
C
E
Ca
CS
60
CS
.
100
0
0
0
0
C
-
40.
2
C
a)
a-
5
60
a)
0
S
80
0
20
40
S
S
CS
#{149}#{149}S
S
Ciliated
2.
Columnar
epithelial
cell
a
Goblet
differentials.
Shown
are
#{149}
S
S
S
S
S
.
S
S
S
SS
5
Ss
S
20
FIGURE
5
S
S&
5.
.
4#{149}
-
#{149}
S
S
S
S
-
0
the
mean
percentages
for the columnar
epithelial
cell types
from the
bronchial
sample
from
the three
subject
groups.
The
ordinate
represents
the percentage
ofthe
total columnar
cells counted.
Solid
bar = chronic
bronchitis;
hatched
bar
asymptomatic
smokers;
and
open
bar = normal
subjects.
5,
2
10
Goblet
20
cell
30
as
a percent
40
50
of total
60
columnar
70
80
cells
FIGURE
4. Correlation
between
goblet
cell proportions
and the
bronchial
sample
neutrophils
for all three
subject
groups.
Ordinate:
goblet
cells
expressed
as a percent
of the total
columnar
cells;
abscissa:
neutrophils
recovered
in the
bronchial
samples
as a
percentage
of the total cells.
CHEST
Downloaded From: http://journal.publications.chestnet.org/pdfaccess.ashx?url=/data/journals/chest/21631/ on 06/18/2017
I 100
I 2 I AUGUST,
1991
391
140
S
120
.5
a,
100
V
a,
a
bronchitis
index
neutrophils.
:
555
tion,
80
S
S
S
S
60
negatively
strongly
of goblet
a,
a
40
S
cell
studied
mality
55
20
20
Goblet
30
cell
FEV1
5. Correlation
percent
predicted
FEy
as percent
as
40
percent
between
for all
predicted;
of the
total
50
of total
goblet
three
70
columnar
goblet
80
cells
med
(r
0.72,
=
and the
Ordinate:
expressed
as
cells.
and
ologic
(Fig
3). The
of columnar
percentage
sample
p<O.OOl)
(r
0.44,
=
tionally,
the percentage
of goblet
with
pack years
of smoking
(r
centage
goblet
cells
normal
nonsmokers
ers). Thus,
increased
with
other
(Fig
cells
ofbronchitis
if changes
with
obstruction,
spirometric
the FEy,
The
lated
percentage
with
the
( Fig
5). Also,
was
no correlation
(r
=
suggesting
was
airflow
including
goblet
the
that
normal
of the
cell
was
(r =
is
ulcers,
goblet
cell
choscopy
bronchial
the
with
-
(r=
ratio
-0.70,
may
age
of goblet
measures
=
of
p<O.OOl).
of the
columnar
lavage
goblet
fluid
cells
demonstrated
in patients
gesting
that
types
tive of the underlying
portions
ofgoblet
cells
392
demonstrate
that
cell
types
present
with
increased
chronic
of cells
lavaged
pathologic
correlated
in bronchial
proportions
bronchitis
are
condition.
positively
of
sug-
representaThe prowith other
chronic
goblet
cell
by which
goblet
are
Increased
that
There
would
are
importance
of
by the study
cells
metaplasia
failure.
could
several
Although
tis and
percentage
FEy1,
obstruction.
strikingly
stronger
such
and
regard,
proportion
the
-
other
the
with
measures
of recovered
change
during
short-term
acute
airway
inflammation.
Chronic
the
Inflammation
Downloaded From: http://journal.publications.chestnet.org/pdfaccess.ashx?url=/data/journals/chest/21631/ on 06/18/2017
may
goblet
declines
-
cell
in
0.74 for
In this
epithelial
in the
among
with Goblet
that
marker
bronchi-
of airway
long-standing
and be less
variations
Second,
Associated
idea
cells is a reliable
with chronic
as BAL neutrophils
(r =
0.44 for BAL neutrophils).
that are goblet
cells may reflect
in epithelial
cell populations
cells
c1ose.#{176}
First,
correlated
than
inflammation
goblet
cells
goblet
to support
of BAL goblet
changes
associated
airflow
was
from
A small
airways
to airway
of bronchioles
resulting
peripheral
airways
and
easily
reasons
contrib-
fold.
cells is much less than
secretion
of mucus
by
mucus
more
several
airflow
metaplasia
cells
may
be relatively
important.
in mucus
production
in the peripheral
be functionally
important
in relation
airways
the
in a series
that goblet
cell
dying
of respiratory
obstruction
the prevalence
of long-term
bron-
found
alter the surface
active
layer
in instability
of the these
0.49,
-
function
to severe
the volume
of epithelial
goblet
that of submucosal
glands,
the
goblet
increase
methodology
cell metaplasia
mild chronic
airflow
autopsy
specimens
that
patients
and
parame-
function,
but
with abnor-
FEy,
percent.
The
is also emphasized
who
in
obstruction)
there
can be used to provide
samples
of
cells sufficient
for analysis.
Eval-
uation
the
study
et al
mechanisms
with
(r
correlated
with the
goblet
cell metaplasia
common
pigment,
similar
goblet
lung
moderate
lumen,
metaplasia,
pathologic
patients
with
et al’#{176}
studied
also showed
a path-
airway
fibrosis,
Using
that
exam-
epithelial
parameters,
cell
individual
reduced
also
the
correlated
with lung
scores
were associated
with
and
to airflow
percent
other
patients
obstruction
ute
percentage
ofthe
squamous
with
The
group,
FEV,/FVC
FEF25-75
of this
and BAL
epithelial
to
have
et al27 derived
ofocciusion
The
from
Nagai
were
the percentage
correlated
obstruction,
results
related
have
and
individual
of lung function.
et al demonstrated
correlated
from
studies
inflammation,
of muscle.
of Karpick
DISCUSSION
The
cells
ofgroups
eight
metaplasia,
of specimens
obstruction.
was
negatively
corre0.74,
p<O.OOl)
nonsmoker
Moreover,
the
directly
airways
Cosio
the degree
as airflow
cells
such
goblet
of goblet
cells
FEy,
percent
in the
and
be
of these
small
to evaluate
cell
was
variables.
To control
for variations
in
as a percentage
of predicted
was used.
negatively
p<0.001),
columnar
manifestations
compared
0. 17, p>O.OS).
cells
in the
clinical
we
with
age,
obstrucgoblet
A number
features.eb0,2627
malities
Wright
4). Addi-
was correlated
p<O.O5,
per-
0.44,
=
epithelial
of bronchial
compared
with pack years in the
and the chronic
bronchitic
smokrecovery
of goblet
cells is asso-
features
To determine
prevalence
increased
could
some
ters were
not well
the total pathologic
percentage
the increased
recovery
of goblet
cells
by lavage
reflective
of the underlying
abnormality
of bronchitis
with increased
goblet
cells present
in the epithelium.
associated
bronchial
cell
ofairfiow
the
function.
of the
score
mucosal
p<O.OOl)
neutrophils
goblet
measures
that
metaplasia
lesions
histologic
cells
cell proportions
subject
groups.
abscissa:
columnar
60
of goblet
cells (as a percentage
cells) also correlated
with the
ciated
of
visual
morphometric
measurements
of lung abnorwith
lung function
using
surgical
or autopsy
amount
index
percentage
the
with
in lung
specimens,
10
chitis
the
5#{149}#{149}
C,.
percentage
the
suggesting
decrements
FIGURE
and
including
reflect
important
underlying
pathologic
changes.
There
are several
lines ofevidence
that the presence
S
C
>
w
inflammation,
Furthermore,
correlated
s
0
a,
C.,
of airway
S
::
V
measures
cells
changes
likely
to
amount
of
the smok-
Cells (Spurzem
at a!)
ers,
BAL
goblet
pack-years
cells
goblet
damage
appears
obtaining
other
to
would
much
single
there
choscopic
biopsy
and
ployed
Thus,
specimens
an averaging
to minimize
problem
lavaged
variability
if random
are
system
sampling
Recent
each
provide
differentials
of
taken,
found
to preparation
is necessary
of normal
subjects
samples.3’
However,
cellular
multiple
would
error.
have
BAL
to be
avoids
and
not
able
both
sputum
samples
and
between
sputum
sample.’2
BAL
avoids
the
samples
pooling
the
chance
are
consistently
aliquots
from
of sampling
multiple
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19
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