A Comparison of the Effects of Membrane
and Bubble Oxygenators on Platelet Counts
and Platelet Size in Elective Cardiac Operations
Horace R. Trumbull, M.D., Jeffrey Howe, Kathy Mottl,
a n d Demetre M. Nicoloff, M.D., Ph.D.
ABSTRACT To compare the effects of membrane
and bubble oxygenators on platelet counts and the
size of circulating platelets, serial hematocrits,
platelet counts, and platelet sizing were measured in
23 patients undergoing elective cardiac operations.
In 10 patients a bubble oxygenator was used and in
13, a SciMed membrane oxygenator. The two groups
were statistically similar with respect to age, weight,
time on bypass, and mean blood flow rates during
bypass.
It was found that platelet counts, when corrected
for hemodilution, did not fall from control levels
during or up to 24 hours after cardiopulmonary
bypass in either group. In both groups, the relative
number of platelets per gram of hemoglobin in-
creased slightly during and after bypass, and this in-
crease was significant in the bubble oxygenator
group. The average size of circulating platelets in-
creased only in the bubble oxygenator group, and
then only in the one-day postoperative sample.
These findings suggest that the membrane oxy-
genator offers no advantage with respect to preser-
vation of platelets during cardiopulmonary bypass
lasting up to 2 to 3 hours.
It is well known that platelet counts fall during
cardiopulmonary bypass. It has been suggested
that the mechanisms for this decrease could be
platelet destruction [l], platelet aggregation and
trapping within the extracorporeal circuit [15],
or platelet sequestration within the liver, the
lung, or other organs [2]. Several authors re-
ported that platelet counts fall less precipitously
when a membrane oxygenator is used instead
of a bubble oxygenator [2, 11, 17, 181, and one
From the Department of Surgery, University of Minnesota,
Minneapolis, MN.
Accepted for publication Dec 14, 1979.
Address reprint requests to Dr. Trumbull, Division of Car-
diac Surgery, University of Arkansas for Medical Sciences,
4301 W Markham St, Little Rock, AR 72205.
52 0003-49751801070052-06$01.25 @ 1979 by Horace R. Trumbull
argument put forth in favor of the routine use of
membrane oxygenators in cardiac operations is
that platelets will be spared [9, 111.
Based on observations in 12 patients, Laufer
and co-workers [8] reported that large platelets
(which are younger and more adhesive) are
selectively removed from the circulation during
the early minutes of cardiopulmonary bypass.
Within 2 hours after termination of bypass,
they found that large platelets are selectively
released into the circulation. The present study
was done to compare the effects of membrane
and bubble oxygenators on platelet counts and
the size of circulating platelets in patients hav-
ing elective cardiac operations.
Material and Methods
Platelet counts and hematocrits were measured
serially in 23 patients having elective cardiac
operations using cardiopulmonary bypass.
Measurements were done prior to bypass; at 5
minutes, 60 minutes, and 120 minutes of
bypass; within 10 minutes of coming off
bypass; on arrival in the recovery room; after 90
minutes in the recovery room; and on the
morning of the first postoperative day. If blood
was used in the priming solution (as it was in
two of the bubble oxygenator perfusions and all
of the membrane perfusions), platelet counts
and hematocrits were also measured on the
prime. Platelet sizing was done on a blood
sample collected prior to bypass, after 90 min-
utes in the recovery room, and on the morning
of the first postoperative day.
Patients scheduled for elective cardiac opera-
tion were assigned to either the membrane or
bubble oxygenator group in a random manner
after the responsible surgeon had indicated a
willingness to have the patient participate in
the study. Ten patients (7 men and 3 women)
were in the bubble oxygenator group and 13 (8
53 Tmmbull et al: Effects of Oxygenators on Platelets

180 calculated from platelet counts measured at

130
120
110
5.50
5.25
5.00
4.75
4.50
4.00
B perimental protocol were compared with con-
Fig 1 . ( A )Absolute platelet counts ( X 109 measured in
Patient 15 without correction for hemodilution. ( B ) The
same data expressed as platelet index after correction for
hemodilution.
men and 5 women) in the membrane oxy-
genator group.
Platelet counts were done by the method of
Rees and Ecker [13]. Platelet sizing was done
using a calibrated microscope ocular microme-
ter with a magnification of 1,000, as described
by Garg and colleagues [6]. Three hundred con-
secutive platelets were counted, and the
number and percentage of platelets measuring
1.0 p to 6.5 p at each 0.5 p increment were re-
corded. Mean platelet size for each sample was
calculated. Individuals doing the platelet counts
and platelet sizing did not know to which
group the samples belonged.
Platelet counts were corrected for hemodilu-
tion by dividing each platelet count by the
simultaneously measured hematocrit, thus
yielding a "platelet index." This then could be
directly compared with other platelet indices
other levels of hemodilution. Figure 1illustrates
the usefulness of the platelet index. Part A
shows absolute platelet counts measured in 1of
our patients plotted without correction for
hemodilution. When compared with B, which
shows the same data expressed as "platelet
index" after correction for hemodilution, it can
be seen that the apparent loss of platelets can be
explained completely by dilution during car-
diopulmonary bypass in this patient.
Platelet indices and sizes measured in each
oxygenator group at different times in the ex-
trol values for that group using the one-sample t
test on differences. The same data were exam-
ined using the two-sample t statistic to compare
the bubble oxygenator group with the mem-
brane oxygenator group.
All membrane oxygenators were SciMed
Kolobow spiral wound membranes, seven were
3.5 m2 in size and six were 2.5 m2. The mem-
brane material was gum in twelve and silicone
rubber in one. The winding tension in all of the
gum membranes was 2.72 kg and in the silicon
rubber unit, 3.18 kg. All membrane units were
run with 50 mm Hg vacuum on the gas phase. A
variety of bubble oxygenators was used. Four
Bentley Q 100 units and three Bentley Q 200 A
units were used. Two Harvey H 1000 oxy-
genators were used; and one Galen Optiflow
adult unit was used.
Details concerning operative procedures, pa-
tients, and pump times and flows are shown in
Table 1. The groups did not differ significantly
in any variable listed. All patients had intrave-
nous administration of Solu-Medrol (methyl

Table 1 . Patient Data:'

Bubble Oxygenator Membrane Oxygenator

Data (N= 10) (N= 13)
Age (yr) 42-68 (55.5) 48-71 (59.7)
Weight (kg) 58.4-102 (78.7) 47-92 (69.1)
Type of operation 8 CAB; 1 MVR + CAB; 1 AVR 13 CAB
Bypass time (min) 52-180 (108.6) 44-129 (96.5)
Flow ( d k g l m i n ) 51.5-68.7 (60.0) 49.5-77.8 (65.9)
"All data except type of operation are given as the range with the mean in parentheses.
CAB = coronary artery bypass; MVR = mitral valve replacement; AVR = aortic valve replacement.
54 The Annals of Thoracic Surgery Vol30 No 1 July 1980

prednisolone sodium succinate), 30 mg per dices measured subsequent to measurement of

kilogram of body weight, prior to the institu-
tion of cardiopulmonary bypass, except 2 (both
in the bubble oxygenator group). They might
have received either 35 mg of dexamethasone or
a placebo instead of methylprednisolone as part
of another study.
Results
The groups did not differ significantly with re-
spect to age, body weight, duration of perfu-
sion, or perfusion flow rates (see Table 1).All
patients in the membrane oxygenator group
underwent only coronary artery bypass opera-
tion. Eight patients in the bubble oxygenator
group had coronary bypass only, 1 had mitral
valve replacement and single vessel coronary
bypass, and 1 had aortic valve replacement.
Platelet index and sizing data are listed in
Tables 2 and 3, and the same data are displayed
graphically in Figures 2 and 3. In the membrane
oxygenator group, platelet indices did not differ
significantly from control values at any time in
the experimental protocol ( p > 0.05). Likewise,
platelet sizes did not differ Significantly from
those obtained before bypass at any point of
observation ( p > 0.05).
In the bubble oxygenator group, all platelet in-
control values were larger than the control
platelet index. This increase was significant at
every point ( p < 0.05) except two: the values
obtained 5 minutes after coming off bypass and
the values obtained on the first postoperative
day ( p > 0.05). However, if platelet indices at
each subsequent time period are compared
with values measured 5 minutes after going on
the pump, no significant differences can be
shown either during the remainder of the per-
fusion or subsequent to perfusion ( p > 0.05).
Platelet sizes measured 90 minutes after arrival
in the recovery room did not differ significantly
from sizes before bypass ( p > O.l), but mean
platelet size on the first postoperative day was
significantly greater ( p < 0.05).
When indices are compared between bubble
and membrane oxygenator groups for each time
period, no significant differences can be shown
( p > 0.05), with the sole exception of the sample
collected just after coming off bypass. Then,
platelet indices were significantly greater in the
bubble oxygenator group ( p < 0.01) (see Figure
2).
In comparing mean platelet sizes, there was
no significant difference between groups either
on the sample obtained before bypass or on that

Table 2 . Platelet Index and Sizing Data for the Membrane Oxygenator Group
Platelet Index Sizing ( p )

Arrive 90 Min 90 Min

Patient Recovery Recovery Before Recovery
No. Control Prime 5Min 60Min 120Min Off Room Room 1D Bypass Room 1D

1 3.37 4.95 3 96 3.79 ... ... 4.05 5.11 ... ... ... ...
2 4.36 2.94 4.64 4.36 ... ... 4.54 4.58 ... ... ... ...
3 4.32 4.22 3.11 4.74 ... ... 4.00 5.32 ... ... ... ...
4 4.89 4.82 5.97 5.77 ... ... 5.03 5.11 ... ... ... ...
7 5.35 6.06 5.48 4.46 ... 4.46 3.68 3.87 4.49 2.48 2.38 2.05
12 3.74 2.85 4.65 4.36 ... 3.30 5.06 4.17 4.39 2.45 2.48 2.38
13 4.62 4.83 5.08 5.11 ... 4.39 4.56 4.79 4.72 2.50 2.54 2.56
14 5.03 4.56 4.75 5.13 5.00 5.00 4.83 4.35 4.13 2.52 2.48 2.54
15 4 13 5.50 4.29 4.10 ... 4.20 4.06 4.45 4.19 2.42 2.43 2.51
16 3.86 3.64 4.40 ... ... 3.93 5.40 3.95 4.66 2.35 2.46 2.36
17 4.00 4.60 4.73 4.19 ... 4.03 3.39 3.40 4.13 2.33 2.48 2.35
18 3.95 4.26 3.48 4.26 3.93 3.93 3.31 3.31 4.03 2.32 2.27 2.31
19 4.60 5.25 4.91 4.30 ... 4.70 4.62 4.32 4.84 2.27 2.20 2.36
z 56.22 58.48 59.45 54.57 8.93 37.94 56.53 56.73 39.58 21.64 21.72 21.42
-
m 4.32 4.50 4.57 4.55 4.47 4.22 4.35 4.36 4.40 2.40 2.41 2.38
SD 0.56 0.93 0.77 0.55 0.76 0.50 0.66 0.63 0.30 0.09 0.11 0.15
SEM 0.16 0.26 0.21 0.16 0.53 0.17 0.18 0.17 0.10 0.03 0.04 0.05
~~

t = sum; 7ii = mean; SD = standard deviation; SEM = standard error of the mean
55 Trumbull et al: Effects of Oxygenators on Platelets

Table 3 . Platelet lndex and Sizing Data for the Bubble Oxygenator Group

Platelet Index Sizing (p)

Arrive 90Min 90 Min

Patient Recovery Recovery Before Recovery
No. Control Prime 5 Min 60Min 120 Min Off Room Room 1D Bypass Room 1D

5 4.55 ... 4.97 4.08 ... 4.27 ... 4.12 5.45 2.21 2.08 2.17
6 4.19 4.84 4.15 4.93 ... 4.37 ... 5.40 5.00 2.35 2.29 2.46
8 3.46 5.44 4.11 4.85 4.88 4.58 5.11 5.14 ... 2.48 2.34 ...
9 4.55 . .. 5.10 4.72 ... 4.37 4.36 4.62 3.25 2.35 2.42 2.51
10 4.08 .. . 5.12 5.13 4.93 5.11 4.29 4.85 5.03 2.38 2.35 2.71
11 4.73 . .. 4.32 4.67 ... 5.10 5.33 5.31 4.72 2.45 2.49 2.45
20 3.60 ... 4.34 4.00 4.24 4.24 3.51 4.10 3.61 2.39 2.38 2.45
21 3.62 ._. 4.09 4.05 4.08 4.42 4.03 3.71 4.00 2.35 2.37 2.46
22 4.07 ... 4.27 4.49 ... 4.49 4.51 4.41 4.72 ... 2.30 2.31
23 3.85 ... 4.39 4.38 ... 5.92 .. . 4.53 4.85 1.57 1.95 ...
1 40.70 10.28 44.86 45.30 18.13 46.87 31.14 46.19 40.63 20.53 22.97 19.52
-
m 4.07 5.14 4.49 4.53 4.53 4.69 4.45 4.62 4.51 2.28 2.30 2.44
SD 0.44 0.42 0.41 0.40 0.44 0.53 0.62 0.56 0.73 0.28 0.16 0.16
SEM 0.14 0.30 0.13 0.13 0.22 0.17 0.23 0.18 0.24 0.09 0.05 0.05

Abbreviations same a s for Table 2

Bubble
l+ Oxygenator

x- Membrane
Oxygenator

P < 0.01
5.0 *

4.5

4.0 I
3.5
Control 5 M i n 60Min 120Min
Fig 2 . Platelet index data for bubble and membrane
oxygenator groups. (SD = standard deviation; RR =
recovery room.)
of the first day ( p > 0.05). Mean platelet size
was significantly larger in the membrane
oxygenator group only on the sample collected
90 minutes after arrival in the recovery room ( p
C 0.05) (see Fig 3).
Comment
After twenty-five years of experience with
clinical cardiopulmonary bypass, we still do not
Platelet
Index
f SD
Off Arrive 90Min 1 Day
RR RR
know precisely what happens to platelets dur-
ing extracorporeal circulation. It is most com-
monly reported that platelet counts fall rapidly
after the institution of bypass, slowly increase
during bypass, and return to or exceed control
levels some days after bypass [lo, 12, 14, 161.
Since none of these studies accounted for the
effect of hemodilution, it is not clear whether
there was a greater loss of platelets than of he-
moglobin. Salzman [141, however, stated that
falls in platelet counts that he observed were too
great to be accounted for by dilution alone.
Only the report of Kolobow and colleagues [7]
56 The Annals of Thoracic Surgery Vol30 No 1 July 1980
Bubble Oxygenator
-- Membrane Oxygenator
2.50 P < 0.05
*
1
2.40
I
2.30
2.20 1
Pre-op 90 Min RR
Fig 3 . Platelet size (p) data for bubble and membrane
oxygenator groups. (SEM = standard error of the
mean; RR = recovery room.)
showed platelet counts remaining in the normal
or elevated range during long-term veno-
venous bypass with and without a membrane
oxygenator in the circuit. Our study supports
the concept that platelets are diluted but not lost
during cardiopulmonary bypass of up to 3
hours. In fact, our data show that when one cor-
rects for the effect of hemodilution, the number
of platelets per gram of hemoglobin actually in-
creases slightly during and after perfusion with
the use of both bubble and membrane oxy-
genators (see Fig 2).
A number of investigators have reported that
fewer platelets are lost with a membrane
oxygenator in the circuit than with a bubble
oxygenator [2, 11, 17, 181. This study does not
support that finding, but confirms the findings
of Dutton [3], Wright [19], and their associates
that platelet counts are equally well preserved
whether a membrane or bubble oxygenator is
used.
It may be of importance that all of our pa-
tients except 2 underwent operation for myo-
cardial revascularization only. Except in the 2
who had valve replacement (both in the bubble
oxygenator group), our use of cardiotomy suc-
T
Platelet
Size k SEM
1Day
tion was nil. This may have influenced our re-
sults. Edmunds and co-workers [4] measured
cardiotomy suction return in a group of 76
pediatric patients and clearly demonstrated that
the loss of platelets during perfusion was di-
rectly related to the percentage of total perfusate
returned by cardiotomy suction.
Laufer and associates [8] studied the influ-
ence of bypass on platelet size using an elec-
tronic sizing apparatus based on the Coulter
counter and reported that early in bypass, large
platelets (which are younger and more adhe-
sive) disappear first from the circulation and are
selectively released into the circulation at the
conclusion of bypass. Using a microscope ocu-
lar micrometer technique of directly measuring
platelets, we could not confirm those findings,
although we did not include sizing of platelets
sampled during bypass as a part of our pro-
tocol. However, on samples taken 90 minutes
after the conclusion of operation, we could not
confirm an increase in the average platelet size
or an increased percentage of large platelets in
either group. Only in the bubble oxygenator
group did we note an increase in mean platelet
size and then only in the sample made one day
postoperatively. The reason for the difference
in these findings is not clear. One possible ex-
planation is that an electronic counter such as
that used by Laufer and co-workers [8] could
57 Trumbull et al: Effects of Oxygenators on Platelets
have counted red cell fragments a n d other d e -
bris produced d u r i n g bypass a s ”large plate-
lets,” a n error avoided i n the direct count-
i n g method. The question deserves further
study.
We wish to emphasize that i n this study w e
d i d not measure any factor of platelet function.
It is known that platelet dysfunction is a regu-
lar consequence of cardiopulmonary bypass.
Friedenberg a n d associates [5] evaluated plate-
let function i n 40 patients before a n d after car-
diopulmonary bypass using both bubble
a n d membrane oxygenators, a n d showed that
platelet aggregation induced by epinephrine,
collagen, a n d adenosine diphosphate was reg-
ularly depressed. They found a decrease in the
uptake a n d release of serotonin labeled with
carbon 14 after bypass, and by electron micros-
copy of platelets after bypass, they showed a
decrease in t h e number of dense granules, in-
creased numbers of vacuoles, and marked
membrane derangements-implying that plate-
lets lose their storage pool d u r i n g cardio-
pulmonary bypass. They believed that there
was no difference i n the degree of induced
platelet dysfunction relative t o t h e type of oxy-
genator used. If that is true, then that fact com-
bined with the findings of this study suggest no
advantage of either membrane or bubble oxy-
genator with respect t o t h e preservation of
platelets or the degree of induced platelet dys-
function i n perfusions of up to 3 hours’ dura-
tion.
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