From www.bloodjournal.org by guest on June 17, 2017. For personal use only.
Mitotic
Indices
and
By
of Human
Cytologic
SVEN-AGE
Bone
Marrow
Distribution
of
KILLMANN,
EUGENE
P. CRONKITE,
VIc’roR
P.
BOND
papers
are
AND
T
HE
OBJECTIVES
In part
)
index
In
part
logic
time
this
in
on the
normal
II,
in the
erroneous
pointed
out.
estimates
in part
III,
tions
of
these
restrictions.
the
time
use
have
of
to
of
Normal
bone
Bone
Mitotic
figures
“twin”
appearance
gen-stained
cell
from
smears,
slides
from
the
cell
with
as interphase
level.
The
With
Ciemsa.
overall
were
type
in mitosis
to
at any
index
figures/’
hemopoietic
Both
the
interphase
possibly
1000
1000
ing characteristics
and
neutrophil
proliferating
marrow
and
there
number
the same
and
compartments
mitotic
line and
mitotic
specific
figures
were
made
as
well
maturation
and
interphase
of a particular
mitotic
index,
cell
e.g.,
of
mitoscs/
100
marrow
cell
mitosesf
cellsf
the
modal
may
exists
to their nuclear
precursors
The
mitotic
aspirates
of
five
differences
cells#{176}
that
classified in respect
local
fraction
mar-
least
from
morphology
suggest
cells.
the
bone
to assign
of
i.e.,
with
in Feul-
At
possible
to cell
and
nuclei
ordinary
number
respect
29
counted
Japa.2
the same
distribution
index,
of
possible
of
previously.1
including
by
to
appropriate
with
x myelocyte
myelocytes/
due
from
cytologic
mitotic
various
of
with
ages
) were
out
errors
an
the
stains
it is not
observer
the
lead
accordance
described
(i.e.,
together
pointed
smears
preparations
specific
in computa-
as
telophase
avoid
method
one
in
applied
between
done
close
as
to
work
may
in
panchromatic
ordinary
and
the
time,
with
squash
classified by
is computed
mitotic
the
compute
to
lying
counted
In these
mitotic
used
were
of cyto-
previous
restrictions
be
males
were
underestimated,
line. Therefore,
cells were
cells
myelocytes,
aspirate
activity.
stained
is
will
healthy
prophase
because,
index
these
proliferation
preparations
meml)rane,
preparations
same
proliferative
nuclear
in
MATERIALS
from
squash
recognizable
no
mitotic
the
to their specific
and
earliest
and
AND
obtained
and
mitotic
computation
appreciated
indices
hemopoietic
were
aspirations
squash
row
in
marrows
marrow
( specific
types
parameters.
mitotic
METHODS
45.
cell
observe
time
specific
parameters
been
Failure
cytologic
observed
threefold:
of specific
not
I. Number
T. M. FLIEDNER
will be presented.
of mitotic
index
for
marrow
which
be
indices
bone
restrictions
will
present
mitotic
human
parameters
field
to
of the
I, data
Cells.
Mitoses
distribution
be
in
four
the
neutrophil
in either
classified
cell
From
the Division
of Experimental
Pathology,
National
Laboratory,
Upton,
LI.,
N.
1’.
This research
was supported
by the U. S. Atomic
Submitted
Dec. 12, 1961;
accepted
for publication
#{176}Fromsquash
preparations.
From Ciemsa
stained marrow
smears.
of
bone
in
the
red
Since
cells
classification
reported
could
sizes
classes
series.
data
according
line
nuclear
cell
size or structure,
cell size. In previously
were
of
dividing
to
be
on
Research
Medical
Energy
Feb.
into
can
labeling,
this
In
four
in
and
not
cytoplasmic
size.4.5
down
cells
series,3
mitosis
rests on
thymidine
nuclear
broken
in
marrow
cell
be
stain-
erythroid
way
the
compartments.
Center,
Brookhaven
Commission.
12,
1962.
743
BLOOD,
VOL.
19, No.
6
(JUNE),
1982
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744
KILLMAN,
Table
1.-Counts
Same
of 1000
Aspiration
CRONKITE,
FLIEDNER
Nucleated
Cells in Separate
Marrow
from Five Healthy
Males-Aspirations
Between
1 P.M. and 8 A.M.
Individual
Time5
TF
TF
3:00
TF
7:00p.m.
Slides
Counted
1:20p.m.
TF
TFf
EPC
10:45
EPC
10:00
Particles
Done
Mitotic
6
6.5
5
10.8
5
13.4
5
7.4
5:00p.m.
5
8.2
5
6.0
p.m.
EPC
10:45p.m.
5
5.8
EPC
11:00p.m.
5
11.8
VPB
10:20p.m.
6
10.5
LF
12:45
JB
8:00
am.
5
7.8
a.ni.
5
8.4
i
#{176}In
TF,
different
aspirations
all marrow
done
were
24-hour
one
during
the
Cells
7.0
5:45a.m.
p.m.
BOWl)
from
Figures/bOO
5
p.m.
AND
8.63
period;
SD
in
±
2.44
EPC,
on
days.
At
\Vith
the mitotic
10 am.,
the
broken
index
morphologic
down
was
criteria
into
three
8.8.
available
for
subcompartments
this
study,
( See
each
these
table
compartments
could
only
be
3).
RESULTS
1. Diurnal
Variation
Previous
work
aspirated
of
degree
work
mal
mitotic
aspirations
to be
ble
highest
in the
of these
indices
2.
of
Ratio
Between
bone
marrow
mitotic
index
samples
( i.e.,
therefore,
normal
red
of
or 50 mitoses
marrow
samples
bone
and
bone
period,
This
marrow
is very
between
aspirations
were
to
to
pool
Myeloid
and
white
hone
marrow
were
counted
aspirated
at
mitotic
however,
activity
was
all
appears
not
discerni-
to note that the mean
(8.6)
close
to the mean
of the mitotic
10 a.m.
parameters
marrow
the
trend,
It is important
observations
time
the
and the over-all
mitotic
index
determined.
1. In one individual
(T. F. ), in whom
hours.
obtained
Erythroid
between
smears
in
nucleated
24 hour
evening
clock
of
one
observations.
marrow
index
The
ratio
from
direct
Twenty-five
12 bone
within
permissible,
mitotic
overall
Therefore,
7
of the day
in table
marrows
bone
that
the
1 p.m.,
1,000
per
late
the
shown
cells
irrespective
of cell type
) with the method
employed
is 9.0 ± 1.0.’ From
anithat
the mitotic
activity
in various
tissues
may
show
of the
around
index
figures
done
in hone
has
and
variations.u
in the
rest
estimates
it appears
the
laboratory
times
tabulated
were
Mitotic
a.m.
diurnal
at different
results
are
Marrow
10
of maturity
it is known
considerable
done
The
in this
between
number
and
of Bone
our
(table
and
be made
previous
1 p.m.
(9.0).
in a following
and
present
For
the
paper,
data
on
2).
Mitoses
cell precursor
mitoses
particles
after
staining
in each
different
was
with
determined
Giemsa.
of two different
smears
times
of the day from
from
seven
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MITOTIC
OF BONE
INDICES
Table
2.-Mitotic
from
MARROW
GES
745
i
Indices
(Mitotic
Figures/1000
Nucleated
Cells)
Counts
of Not Less Than
5000 Cells in 21 Different
Marrow
Aspirations
from Nine Healthy
Males
Sum
Number
Aspirations
Individual
of
Determined
Bone
of
Mitotic
Indices
Each
Individual
in
Mean
of
Mitotic
Indices
TF
7
61.4
8.77
EPC
5
40.5
8.1
VPB
2
18.9
9.45
LF
2
17.0
8.5
JB
VP
PH
CBS
SAK
1
1
1
1
1
8.4
9.2
9.0
10.3
8.0
21
Weighted
(8.4)
(9.2)
(9.0)
(10.3)
(8.0)
8.70±
1.88
8.86
Mean
±
0.73
Mean
healthy
males.
Among
were
mitoses
in myeloblasts,
700
in erythroid
promyelocytes
thus
mitoses
precursors,
and
counted,
28.2
neutrophil
69.4
( SD ) were
mitoses
in eosinophil
myelccytes,
cells.
A comparison
of these
percentages
other
in
between
10 a.m.
nificant
differences.
3.
Mitoses
Two
were
ing
1 p.m.
in Different
smears
to cell
are
each
and
shown
during
the
rest
1.9
0.5 per
in bone
of
the
.96
±
( SD)
cent
mitoses
per cent
cent
were
mitoses
marrows
aspirated
day
showed
no
aspirates
from
six healthy
25 or 50 cells
in mitosis
were
classified
A total
mitotic
slide,
maturity.
in table
and
per
( SD ) were
sig-
of Maturation
of 11 bone
In each
type
and
Stages
from
examined.
results
and
5.74
±
5.18 per cent
myelocytes,
±
marrow
of 650
cells
were
males
accord-
evaluated;
the
3.
DIscussIoN
The
Problem
In
of Diurnal
a previous
report
some
Mitotic
estimates
turnover
used
were
not
a 24-hour
period.
individual
24-hour
(T.
period
F.)
in whom
would
suggest
hours;
however,
no
order
to establish
in human
beings,
pirations
tions.
the
within
The
day
main
was,
In
such
reason
however,
representative
the
study,
diurnal
probably
or
for
to
present
48-hour
studying
ascertain
can
be
found
changes
be necessary
period
the
whether
in
in
bone
the
the
rest
under
highly
mitotic
index
figure
activity
in
were
obtained
a peak
during
in
human
samples
mitotic
observations
of bone
marrow
to do serial
the
normal
marrow
that
the mitotic
the day and that
of
the
six marrow
samples
such
a variation
with
out
it will
a 24-
indices
necessarily
tendency
or rule
mitotic
times
between
10 a.m. and 1 p.m.’
It was realized,
however,
of the marrow
need
not remain
constant
throughout
during
on
of
drawn
figures
based
Index
marrow
the
made
of the
bone
index
were
Variation
of
the
the
data.
of
In
mitotic
activity
bone
marrow
as-
standardized
at
one
during
one
the evening
different
8.97
conditimes
mitoses
of
per
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746
KILLMAN,
Table
3.-Distribution
CRONKITE,
of 650 Mitotic
Cells from Normal
Bone
to Cell Type and Stage
of Maturation
_____-
Number
Polychromatic
normoblast
Erythroid
18
1
36
2
myelocyte
Eos.
#{176}These mitotic
1
2
have
of the
be
the
data
nucleated
Mitotic
Activity
can be
in bone
as
bone
calculated
marrow
as used
series
figures
differ
report
erythroid
precursors)
(of
mitoses
1,056
myeloid).
On
in the normal
mitoses
and
for
28.2
and
what
observed,
cent
75.0
per
or
2.50
2.44
or
of the five
±
throughp.m.
may
activity
we
figure
throughout
have
chosen
of 8.86
to
mitoses
per
loss
to neutrophil
in ordinary
69.4
the
of
calculated
cent
were
bone
5.74
±
cent
data
(67
be
preferential
of erythroid
of erythroid
and neutrophil
from
the squash
preparations
per
5.18
White8
therefore,
69.4 per
mean
is constant
10 a.m.-1
marrow
is no
index),
can
of all
following,
use the
value.
of erythroid
700 mitoses
±
study
weighted
Granulocytopoiesis
from
and
per
the
the
there
mitotic
Dacie
the average,
bone
marrow,
28.2
and
considerably
by
of
in
smears
and
at in a previous
If mitotic
time
drawn
between
made
the ratio
Among
The
samples
was
8.63
mean
mitotic
indices
the relative
contributions
mitotic
index
obtained
from
smears.
erythroid
marrow
of the
in table
2 and
normal
average
marrow
aspirates
the
am.
mean
activity.
representative
as indicated
cells
as the
) arrived
samples
mitotic
to be
mitoses,
then
to the overall
normoblasts.
time
interval.
in marrows
estimates
(same
These
1 p.m.
24-hour
in this
indices
in the
with
polychromatic
in Ergthropo-iesis
If in ordinary
or myeloid
precursors
of
1 p.m.-8
as the
regarded
For
all our
size
( 10 a.m.-
cells
studied
mitotic
day,
day.
1,000
the
indices
in the
1.11 if expressed
therefore
pool
13
cells
cells
nucleated
7.1
182
cell
representative
±
total
myelocytes
Reticular
the
128
precursors,
Lymphoid
individuals
out the
9.5
452
Myeloblast
Neutrophil
mitotic
8.77
294
37
total
Promyelocyte
Neutr.
1,000
4.1
257
normoblast
precursors,
According
1
127
Orthochromatic
BOND
Relative
Frequency
of Mitoses
31
normoblast
AND
Marrows
of Mitoses
Proerythroblast
Basophilic
was
FLIEDNER
in
of Japa2
100
per
cent
but
the
erythroid
are
and
of the 8.86 mitoses/1,000
cent or 6.15 mitoses/1,000
mitoses/1,000
are
found
precursors.
in agreement
counted
data
mitoses
smears
were
neutrophile
mitoses
from
precursor
marrow
were
in
of Videbaek9
25.0
per
cent
nucleated
cells
are erythroid
neutrophil
precursor
mitoses.
Distribution
are
of ?Iitoses
on
The
relative
frequencies
listed
in table
3. Apart
Different
Maturation
of mitoses
in
from
difficulties
Levels
cells
at different
maturation
in cytologic
identification
levels
of very
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MITOTIC
INDICES
immature
Myeloblast
OF
BONE
cytoplasm
blue
without
difficulties,
it is possible
have
erroneously
been
in small
in
( i.e.,
blasts.
In
the
of
normal
nuclear
the
in the
normal
values
reported
in
late
is
blasts
do
not
by
show
synthesize
“orthochromatic”
the
mature
cells
about
two-thirds
more
primary
DNA.3
To
than
of
that
the
phil
series
of
erythroid
series
mitoses
the
observed
ratio
a proerythroblast,
further
of
In other
cell
generations,
will
be
cell,
ratio
=
generation,
1:
the
both
cells
of prc’erythroblast
1:14.
This
means
precursor
cells
four
1:15,
cells
into
tween
four
time
increases
the
and
plus
erythroid
five
with
which
result
division
interphase
is 1:
to
cell
will
in
to
third
mitoses
in
its
division
in
precursor
an
orderly
consecutive
divisions
maturation,
the
number
Similar
in the
of
etc.,
so
by
is
that
will
mitoses
value.
In
this
divisions
prois not a stem
differentiate,
and
cell
1:
the
(2+4+8)
ervthroid
which
considerations
neutrophile
be
mitotable
erythroid
mitoses
will be
in the recognizable
stem
the
the
will
four
observed
consecutive
13.6,
scheme
generations
unrecognized
pooi.
pro-
1:
mitoses
goes
through
five consecutive
correct.
If the proerythroblast
from
=
each
proerythroblast
generation,
two in
to other
to the
neutroof
differentiation
an
is followed
mitoses
the
ratio
for
and
for
vary
the red cell series,
mitosis
will remain
destined
successive
is close
not
+ 9.5)
of
to
) suggest
3
and
generation,
proerythroblast
which
ds
( table
neutrophile
constant
the
rise
observed
other
be
time
by
giving
representing
time
(4.1
of
cells.
the most
mitoses
divisions
mitoses
hence
dimensions
mitoses
The
mitoses
to other
erythroid
four
consecutive
divisions
one
and
counts,
mitotic
of
divisions.
of proerythroblast
=
a red cell on an average
that
the assumptions
are
then
If
consecutive
mitotic
if the
ratio
(1+2+4+8)
the
myelocyte
mitoses
sister
mitoses
words,
a view
normoblasts
the following
would
be observed:
will be one mitosis
in the first daughter
prcerythroblast
1:1:2:4:8.
event,
vided
its
mitoses
normo-
cytoplasmic
is the ordinary
stem
cell
emerge
from
a proerythroblast
With
We
be
thymidine
of
mitoses.
five
and
cells.
“orthrochromatic”
and
and
erythroid
whereas
daughter
ratio
to
tritiated
frequencies
of myeloblast
multiplication.
of proliferation,
mitosis
there
second
myeloid
other
normoblasts
also classified
as polychromatic
of mitoses
are contributed
contains
to
red
fact
cells,
hemoglobinization,
with
mitoses
a
of nucleated
small
nuclear
relative
1:9.1.
If the proerythrohlast
one of the two cells which
and
advanced
( or five ) consecutive
four
erythrohlast
all
the
of these
polychromatic
erythroid
level,
precursors,
comparability
with
normobetween
eiythroid
typical
assure
encountered
discrepancies
classes
labeling
dividing,
of all
two-thirds
maturation
that
normoblast
were
largest
numbers
the
of
with
fact
any
capable
with
and
the
infrequently
cells
seen
) “orthrochromatic”
“orthrochromatic”
normoblasts
polvchromatic
In table
3,
were
in classifications
different
normoblasts
supported
not
for
with
morphologic
of other
primitive
No mitoses
were
considerable
variations
in large
polychromatic
which
do
mitoses
wide
is possible.
in diameter
t
inherent
mitoses
mitoses.
differentiation
explains
cells
15
cf the
mitoses
are
mitotic
about
Because
there
cytoplasmic
in part
these
of
cells
normoblasts
marrow
which
consider
classification
granules.
polychromatic
bone
and
),
as mitotic
normoblasts;
size
747
I
that in some
instances
classified
as myeloblast
“orthochromatic”
large
CELLS
cells
( myeloblasts
were
defined
mitotic
mitoses
a pale
MARROW
feeds
suggest
be-
series.
If mitotic
divisions
may
be
From www.bloodjournal.org by guest on June 17, 2017. For personal use only.
748
CRONKITE,
KILLMAN,
Table
4.-Mean
Individuals
Bone
Studied,
Marrow
Relative
Differential
Compartment
Count
Number
Pr. 1000
Number
of
Cells in
Mitosis
pr. 1000
Nucleated
CeilsI
Cell
Compart-
Frequency
of
Mitosest
ment
Smear
Type
Relative
Relative
Particle
AND
BOND
of 500 Cells in Each of Six of the
Sizes,
and Specific
Mitotic
lndices
Nucleated
Cells in
Bone Marrow
FLIEDNER
Size
Specific
Mitotic
Index
(fraction
in mitosis)
Nlyeloblast
10
1.00
1.0
0.249
Promyelocyte
33.7
3.37
2.0
0.498
0.0249
0.0148
16.30
7.1
1.778
0.0109
36.14
Myelocyte
163.0
Non-dividing
marrow
granulocytes#{176})
0
0
0
1.tX)
1.0
0.422
0.0253
35.0
2.10
4.1
1.729
0.0494
70.7
4.23
9.5
3.998
0.0565
6.11
0
0
361.4
16.7
Proerythrohlast
-
Basophilic
normoblast
Polychromatic
normoblast
Orthochrornatic
normoblast
U
102.0
Metamyelocytes
I From table
I Calculated
total
to
§Specific
less.
relative
UI(l
mitotic
6.15
neutrophils.
cells
table
=
not
4, the
frequency
total
index
marrow
In
segmented
3.
from
neutrophile
Bone
nuirrow
of
erythroid
fraction
pertinent
of
mitoses
mitoses
specific
to the
specific
on
pr.
cell
present
mitotic
different
maturation
1000
nucleated
cells.
type
in
study
( the
index
mitosis
were
at
any
excluded
fraction
levels
2.50
time.
from
of one
and
the
table.
particular
cell
type
in mitosis
at any time ) is tabulated.
The
highest
specific
mitotic
index
is found
in the most
immature
cells of the neiitrophil
series
and in the most
mature
cells
of the
dividing
erythroid
series.
The
mitotic
index
is much
greater
in the
erythroid
than
in the
neutrophil
series,
the specific
mitotic
index
in the
The
The
most
lishing
are
former
present
likely
the
recognized
than
smears.
Most
gross mitotic
earlier
indices
study.
The
From
the
present
and
basophilic
1:1.86.
is that
index
of
greater
than
the
the
bone
bone
because
they
distribution
work
in the
technic
marrow,
marrow
latter.
reported
squash
who
The
reason
for
data,
this
normoblasts
ratio
is 1:13.5;
were
this
specific
from
this overall
Giemsa
stained
counted
have
cells
the
separately
and found
a higher
mitotic
index
index
in the more
mature
red cell precursors
probable
for
mitotic
mitotic
indices
granulocytopoietic
of Schwarz’5
values.944’18
used
more
smears.
were
computed
of mitoses
in
reports
of hemopoietic
of erythropoietic
and
is the
than
previously
with
mitotic
and
interphase
cells.
mitoses
to other
normoblast
blasts
be
times
higher
in conventional
exception
sification
of
proerythrohlast
to five
are
mitotic
are high
cytologic
of proerythroblasts
blasts
and a lower
present
up
indices
explanation
overall
ic indices
then
index
and
the
A notable
being
mitotic
is differences
in
mitotic
cytologic
however,
if mitoses
group,
index
in proerythrothan
in the
thus
found
the
to be approximately
in one
mitotmitotic
marrow
dealt
with
as a whole.
Schwarz
mitoses
combined
estabfigures
clasratio
of
1:2.
in proerythrothe
ratio
would
From www.bloodjournal.org by guest on June 17, 2017. For personal use only.
MITOTIC
INDICES
From
the
are
possible.
will
be
OF
BONE
present
data,
The
use
examined
putations
by other
MARROW
estimates
restrictions
in the
will be
methods.
some
and
of
paper.17
and
bone
of mitotic
following
presented
749
CELLS
the
time
for
a third
In
results
marrow
indices
paper,’8
compared
parameters
such
computations
the
with
actual
estimates
com-
obtained
SUMMARY
1. The diurnal
studied.
A diurnal
for
further
2. Data
variation
variation
study.
on the
turation
stages
bone
distribution
are
marrow,
of mitotic
has not
the
index
been
of hone
presented.
indices
this
1. Esseva
studiate
Le
remane
aperte
2. Es
Ic variation
question
de
pro
grossier
indice
le vane
typos
de
super
cellula
mitotic
the
on
gross
cell
marrow
remains
cell
lines
mitotic
types
are
has
been
subject
and
index
maof
the
computed.
del
indice
variation
mitotic
diurne
de
non
human
esseva
medulla
resolvite
sed
additional.
datos
typos
but
INTERLINGUA
diurne
possibile
studios
presentate
secundo
tin
IN
bone
mitoses
and
of various
SUMMARIO
ossee.
marrow
From
mitotic
of human
demonstrated
Ic distribution
e stadios
del
de
medulla
de
mitoses
maturation.
ossee,
in
A base
le indices
le medulla
de
mitotic
iste
ossee
datos
e del
es computate
pro
de cellula.
REFERENCES
1. Fliedner,
T. M.,
V.
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From www.bloodjournal.org by guest on June 17, 2017. For personal use only.
1962 19: 743-750
Mitotic Indices of Human Bone Marrow Cells. I. Number and Cytologic
Distribution of Mitoses
SVEN-ÅGE KILLMANN, EUGENE P. CRONKITE, T. M. FLIEDNER and VICTOR P. BOND
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