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Randomized trial

Randomized clinical trial of the effect of pneumoperitoneum on


cardiac function and haemodynamics during laparoscopic
cholecystectomy
J. F. Larsen1 , F. M. Svendsen2 and V. Pedersen3
Departments of 1 Surgical Gastroenterology, 2 Anaesthesiology and 3 Cardiology, University Hospital of Aalborg, Aalborg, Denmark
Correspondence to: Dr J. F. Larsen, Poppelvej 2 A, 9000 Aalborg, Denmark (e-mail: jfl@dadlnet.dk)

Background: Conventional laparoscopic cholecystectomy (CLC) with carbon dioxide pneumoperitoneum may cause major cardiovascular changes. The aim of this study was to evaluate the effect of
carbon dioxide pneumoperitoneum and positional changes on haemodynamics and cardiac function in
patients assigned randomly to CLC or gasless laparoscopic cholecystectomy (GLC).
Methods: Fifty patients with American Society of Anesthesiologists physical status I and II were randomly
allocated to CLC (28 patients) or GLC (22). Left ventricular end-diastolic and end-systolic diameters,
fractional shortening and cardiac output were determined by transoesophageal echocardiography.
Measurements were performed before (phase 1) and 10 and 30 min (phases 2 and 3 respectively)
after pneumoperitoneum or abdominal wall traction, and after desufflation or release of abdominal wall
traction (phase 4) in supine, Trendelenburg and reverse Trendelenburg positions.
Results: Mean diastolic diameter, systolic diameter, mean arterial pressure and heart rate
were significantly higher, and fractional shortening was significantly lower, with carbon dioxide
pneumoperitoneum than with the gasless procedure during phases 2 and 3. There were no significant
differences in cardiac output between the two groups.
Conclusion: Carbon dioxide pneumoperitoneum was associated with increased preload and afterload
in patients undergoing laparoscopic cholecystecomy. It also decreased heart performance (fractional
shortening), but did not affect cardiac output.

Paper accepted 11 March 2004


Published online 14 May 2004 in Wiley InterScience (www.bjs.co.uk). DOI: 10.1002/bjs.4573

Introduction

Laparoscopic surgery involves less trauma than open


operation. However, there is concern about the cardiovascular changes that may be induced by the carbon
dioxide pneumoperitoneum needed to create workspace1 .
Increases in heart rate, mean arterial blood pressure
(MAP) and systemic vascular pressure are the main
haemodynamic changes associated with carbon dioxide
pneumoperitoneum2 6 , but its effect on heart performance
is less certain; cardiac output (CO) has been reported
to decrease2,7 9 , remain unchanged10 13 or increase14 .
CO is determined by preload, afterload, contractility and
heart rate, which may all be affected by the carbon
dioxide pneumoperitoneum. Other factors may also influence haemodynamics during laparoscopy, including the
Copyright 2004 British Journal of Surgery Society Ltd
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anaesthetic, the position of the patient during operation,


intra-abdominal pressure and cardiopulmonary status. In
the light of this, it is understandable that consistent changes
in cardiac function have not been recorded.
Gasless laparoscopy with abdominal wall retraction is
an alternative to pneumoperitoneum during laparoscopic
abdominal surgery15 17 . The benefit of this approach is
that haemodynamic and cardiac effects of carbon dioxide
pneumoperitoneum are largely avoided.
The aim of this study was to evaluate the effect of
pneumoperitoneum and positional changes on haemodynamics and cardiac function, in patients assigned randomly
to conventional laparoscopic cholecystectomy with carbon dioxide insufflation (CLC) or gasless laparoscopic
cholecystectomy (GLC).
British Journal of Surgery 2004; 91: 848854

Effect of pneumoperitoneum on haemodynamics and cardiac function

Patients and methods

Patients with symptomatic gallstones who fulfilled the


inclusion criteria were randomly allocated to either
CLC or GLC. These criteria included admission for
elective surgery, American Society of Anesthesiologists
(ASA) physical status I or II, age over 18 years and
body mass index 30 kg/m2 or less. All patients gave
written informed consent. Patients with acute pancreatitis,
cholecystitis, cholangitis, blood disease, rheumatic disease,
acute infectious disease, renal or liver disease were excluded
from the study. The allocation sequence was generated by
random numbers. Patients were allocated randomly by
opening sealed envelopes on the day of operation. The
intervention assignments were unknown to the patients
and the nursing staff. The local ethics committee approved
the study.

Anaesthesia and medication


Gentamicin 240 mg was given intravenously to all
patients 1 h before the procedure. Patients were not
premedicated, to avoid interference with pulmonary and
haemodynamic functions. Isotonic saline 10 ml/kg was
infused intravenously before induction of anaesthesia and
continued at 5 ml per kg per h. Anaesthesia was induced
with a bolus of midazolam 2 mg and propofol 25 mg/kg.
Patients received fentanyl 5 g/kg during the first hour
and 25 g/kg thereafter. Anaesthesia was maintained
with propofol 12 mg per kg per h. Muscle paralysis
was facilitated with cisatracurium 01 mg/kg for tracheal
intubation and further muscle relaxation was monitored by
a nerve stimulator. Patients were ventilated by means of a
TM
Servo 900 C respirator (Siemens, Solna, Sweden) with a
tidal volume of 7 ml/kg, at a rate of 12 breaths per min and
fraction of inspired oxygen of 030; this was maintained
during the operation. Ondansetron hydrochloride 4 mg
was given intravenously 30 min before the expected time
of extubation, and neostigmine methylsulphate 25 mg
and glycopyrronium bromide 05 mg was administered
to prevent non-depolarizing neuromuscular blockade.

Surgery
Three surgeons experienced in both procedures performed
all operations. CLC was performed using carbon dioxide
pneumoperitoneum at a pressure of 12 mmHg, with
two 10-mm ports and two 5-mm ports. In the gasless
group, two curved steel needles were inserted into the
subcutaneous space and attached to a mechanical arm
fixed to the operating table (Laparotensor ; Lucini, Milan,
Italy). A minilaparotomy (15 mm) was performed through
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849

the umbilicus. An unvalved 10-mm port was inserted,


and a further 10-mm and two 5-mm unvalved ports. By
elevation of the abdominal wall a working chamber was
created. GLC and CLC were performed using identical
instruments and technique. Cholangiography was not
performed routinely. Perioperative complications such as
bleeding and perforation of the gallbladder were noted.

Data collection
Primary outcome measures included left ventricular enddiastolic and end-systolic diameters, fractional shortening
and CO, which were determined by transoesophageal
echocardiography (TOE). Secondary outcome measures
were MAP and heart rate. TOE was performed by insertion
of a 5-MHz two-element annular, monoplane probe
(TN100047; Vingmed, Horten, Norway). Echocardiography included examination of the transgastric short-axis
view at the mid-papillary level, mitral annulus diameter
at diastole and mitral flow curves at the mitral annular
level. All images were recorded on to videotape by
one investigator and later analysed by the same person,
who was blinded to the treatment received. Fractional
shortening of the left ventricle of the heart (diastolic
diameter systolic diameter/diastolic diameter) and CO
were calculated. CO was calculated by multiplying the
time velocity integral of the mitral flow (TVI) by the
cross-sectional area of the mitral ostium (A) and the heart
rate (HR): CO = TVI A HR. Data were collected
after induction of anaesthesia, but before carbon dioxide
insufflation or abdominal wall traction (phase 1), 10 and
30 min after carbon dioxide insufflation or abdominal
wall traction (phases 2 and 3 respectively), and 10 min
after exsufflation or release of wall traction (phase 4).
All measurements were performed with the patient in the
supine, 20 Trendelenburg and 20 reverse Trendelenburg
positions. A 5-min stabilization period was allowed between
each change in position.

Statistical analysis
The sample size was calculated assuming an expected
difference in mean fractional shortening of 01, expected
standard deviation 010, = 005 and power = 090. A
sample size of 46 patients was calculated to be sufficient to
detect these differences.
Results are reported as mean(s.d.). Statistical analysis was
performed using the Jandel Sigmastat version 2.0 statistical
package (SPSS, Chicago, Illinois, USA). Demographic
data were compared using the unpaired Students t-test.
Three-way ANOVA was used to compare differences
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British Journal of Surgery 2004; 91: 848854

850

J. F. Larsen, F. M. Svendsen and V. Pedersen

Results

Fifty-four patients were enrolled in the study. The trial


profile and TOE measurements performed in the four
phases and three positions are shown in Fig. 1. Four
patients were excluded from the study owing to technical
problems with the echocardiograph during surgery. Four
gasless operations were converted, three to open surgery
because of empyema of the gallbladder and one to
carbon dioxide pneumoperitoneum owing to reduced
exposure due to protrusion of the transverse colon. One
CLC was converted to open surgery in a patient with
chronic cholecystitis and Mirizzis syndrome. There was
no significant difference in conversion rate between groups
(P = 0182). Patient data were included in the analysis until
the time of conversion. The two groups were comparable
with respect to age, sex and body mass index (Table 1). The
duration of CLC tended to be longer than that of GCL,
although the difference was not significant. The rates of
perforation of the gallbladder were 10 of 28 and seven of 22
respectively (P > 0050, 2 test). No major intraoperative
complications occurred in either group. In the CLC group
TOE was difficult to perform during phases 2 and 3 in the
reverse Trendelenburg position.

Diastolic diameter
Diastolic diameter was significantly higher in the CLC
group than in the GLC group during operation, allowing
Table 1

Randomized
(n = 54)

Missing
data (n = 2)

CLC
Phase
Phase
Phase
Phase

Allocated
to GLC
(n =24)

Analysed
CLC
(n =28)

Analysed
GLC
(n =22)

S
27
24
24
27

1
2
3
4

GLC (n = 22)

19 : 11
49(11)
24(8)
86(32)

15 : 7
48(11)
26(2)
102(36)

Values are mean(s.d.). CLC, conventional laparoscopic cholecystectomy;


GLC, gasless laparoscopic cholecystectomy. There were no significant
differences between groups.

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Published by John Wiley & Sons Ltd

R
27
14
10
26

GLC
Phase
Phase
Phase
Phase

S
20
22
21
18

1
2
3
4

T
19
21
21
19

R
20
20
20
18

for the effects of differences in positions and phases


(F = 800, P = 0005, three-way ANOVA) (Fig. 2). During
surgery changes in position did not significantly affect
diastolic diameter in the two groups and no significant
changes in diastolic diameter were recorded comparing
phase 2 with phase 3.
CLC
GLC

50
40
30
20

T
Phase 1

CLC (n = 28)

T
27
28
25
24

Missing
data (n =2)

Trial profile and transoesophageal echocardiographic


measurements. Phase 1, before pneumoperitoneum or
abdominal wall retraction; phase 2, 10 min after
pneumoperitoneum or abdominal wall traction; phase 3, 30 min
after pneumoperitoneum or wall traction; phase 4, 10 min after
desufflation or release of wall traction. CLC, conventional
laparoscopic cholecystectomy; GLC, gasless laparoscopic
cholecystectomy; S, supine position; T, Trendelenburg position;
R, reverse Trendelenburg position

Demographic data

Sex ratio (M : F)
Age (years)
Body mass index (kg/m2 )
Operating time (min)

Allocated to
CLC
(n =30)

Fig. 1

Diastolic diameter (cm)

between and within more than two groups. The following


variables were analysed: procedure (pneumoperitoneum
or traction), position (supine, Trendelenburg or reverse
Trendelenburg) and duration of pneumoperitoneum or
traction. If a difference was found between the groups, the
StudentNewmanKeuls method for pairwise multiple
comparison was used to isolate the group or groups that
differed from the others. Missing data were treated by
using a general linear model. P < 0050 was considered
statistically significant.

T
Phase 2

T
Phase 3

Phase 4

Mean(s.d.) left ventricular end-diastolic diameter


measured during conventional laparoscopic cholecystectomy
(CLC) and gasless laparoscopic cholecystectomy (GLC). Phase
1, before pneumoperitoneum or abdominal wall retraction; phase
2, 10 min after pneumoperitoneum or abdominal wall traction;
phase 3, 30 min after pneumoperitoneum or wall traction; phase
4, 10 min after desufflation or release of wall traction. S, supine
position; T, Trendelenburg position; R, reverse
Trendelenburg position

Fig. 2

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British Journal of Surgery 2004; 91: 848854

CLC
GLC

40
30
20
10

Phase 1

851

Fractional shortening

Systolic diameter (cm)

Effect of pneumoperitoneum on haemodynamics and cardiac function

T
Phase 2

Phase 3

CLC
GLC

06
05
04
03
02

Mean(s.d.) left ventricular end-systolic diameter measured


during conventional laparoscopic cholecystectomy (CLC) and
gasless laparoscopic cholecystectomy (GLC). Phase 1, before
pneumoperitoneum or abdominal wall retraction; phase 2,
10 min after pneumoperitoneum or abdominal wall traction;
phase 3, 30 min after pneumoperitoneum or wall traction; phase
4, 10 min after desufflation or release of wall traction. S, supine
position; T, Trendelenburg position; R, reverse
Trendelenburg position

Fig. 3

Phase 2

Phase 3

Phase 4

Mean(s.d.) fractional shortening measured during


conventional laparoscopic cholecystectomy (CLC) and gasless
laparoscopic cholecystectomy (GLC). Phase 1, before
pneumoperitoneum or abdominal wall retraction; phase 2,
10 min after pneumoperitoneum or abdominal wall traction;
phase 3, 30 min after pneumoperitoneum or wall traction; phase
4, 10 min after desufflation or release of wall traction. S, supine
position; T, Trendelenburg position; R, reverse
Trendelenburg position

Fig. 4

Cardiac output (l/min)

Systolic diameter
During operation systolic diameter was significantly higher
in patients who had carbon dioxide pneumoperitoneum
than in those who had a gasless procedure, allowing for the
effects of differences in positions and phases (F = 1129,
P < 0001, three-way ANOVA) (Fig. 3). During surgery
changes in position did not significantly affect systolic
diameter in the two groups and no significant changes in
systolic diameter were recorded comparing phase 2 with
phase 3.

Phase 1

Phase 4

CLC
GLC

80
70
60
50
40
30

T
Phase 1

T
Phase 2

T
Phase 3

Phase 4

Mean(s.d.) cardiac output measured during conventional


laparoscopic cholecystectomy (CLC) and gasless laparoscopic
cholecystectomy (GLC). Phase 1, before pneumoperitoneum or
abdominal wall retraction; phase 2, 10 min after
pneumoperitoneum or abdominal wall traction; phase 3, 30 min
after pneumoperitoneum or wall traction; phase 4, 10 min after
desufflation or release of wall traction. S, supine position; T,
Trendelenburg position; R, reverse Trendelenburg position

Fig. 5

Fractional shortening
Fractional shortening was significantly lower during CLC
(phases 2 and 3) than during GLC, allowing for the
effects of differences in positions and phases (F = 756,
P = 0006, three-way ANOVA) (Fig. 4). Further analysis
revealed significantly decreased fractional shortening in
the reverse Trendelenburg position in the CLC group
compared with the gasless group (F = 412, P = 0017)
whereas no differences were registered in the supine or
Trendelenburg positions.

decrease from Trendelenburg to reverse Trendelenburg


position.

Cardiac output

Heart rate

There were no significant differences in CO between the


groups, allowing for the effects of differences in positions
and phases (F = 0114, P = 0948, three-way ANOVA)
(Fig. 5). Positional changes followed the same pattern in
both groups, irrespective of the phase: a significant increase
from supine to Trendelenburg position and a significant

The heart rate was significantly higher in the CLC group


than in the GLC group, allowing for the effects of
differences in positions and phases (F = 2394, P = 0006,
three-way ANOVA) (Fig. 6). It did not change significantly
during operation (phases 2 and 3) compared with the rate
in phase 1.

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British Journal of Surgery 2004; 91: 848854

Heart rate (per min)

852

J. F. Larsen, F. M. Svendsen and V. Pedersen

Discussion

CLC
GLC

90
80
70
60
50
40

Phase 1

Phase 2

Phase 3

Phase 4

Mean(s.d.) heart rate measured during conventional


laparoscopic cholecystectomy (CLC) and gasless laparoscopic
cholecystectomy (GLC). Phase 1, before pneumoperitoneum or
abdominal wall retraction; phase 2, 10 min after
pneumoperitoneum or abdominal wall traction; phase 3, 30 min
after pneumoperitoneum or wall traction; phase 4, 10 min after
desufflation or release of wall traction. S, supine position; T,
Trendelenburg position; R, reverse Trendelenburg position

Fig. 6

Mean arterial pressure

Mean arterial pressure (mmHg)

During operation (phases 2 and 3) the MAP was significantly higher with carbon dioxide pneumoperitoneum than
during gasless procedures, allowing for the effects of positional changes and time (F = 1900, P < 0001, three-way
ANOVA) (Fig. 7). The two groups showed the same pattern of changes, irrespective of phase: a significant increase
from supine to Trendelenburg position and a significant
decrease from Trendelenburg to reverse Trendelenburg
position.

CLC
GLC

120
100
80
60
40
20

T
Phase 1

T
Phase 2

T
Phase 3

Phase 4

Mean(s.d.) mean arterial pressure measured during


conventional laparoscopic cholecystectomy (CLC) and gasless
laparoscopic cholecystectomy (GLC). Phase 1, before
pneumoperitoneum or abdominal wall retraction; phase 2,
10 min after pneumoperitoneum or abdominal wall traction;
phase 3, 30 min after pneumoperitoneum or wall traction; phase
4, 10 min after desufflation or release of wall traction. S, supine
position; T, Trendelenburg position; R, reverse
Trendelenburg position

Fig. 7

Copyright 2004 British Journal of Surgery Society Ltd


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This randomized study has allowed evaluation of the


pathophysiological consequences of carbon dioxide pneumoperitoneum and positional changes during laparoscopic
surgery. Carbon dioxide pneumoperitoneum increased
the afterload, preload and decreased heart performance,
compared with the gasless technique, during laparoscopic
cholecystectomy in patients with ASA physical status III,
but it did not affect CO. These effects were most pronounced in reverse Trendelenburg position.
The performance of the left ventricle as a pump depends
on contraction of the sarcomeres in the myocardium
and the loading conditions. Myocardial shortening is
determined by four factors: preload, afterload, contractility
and heart rate. Preload is proportional to the stretch of the
myocardium before stimulation. Within the physiological
range, the greater the preload, the stronger the contraction
and the greater the extent of shortening. Diastolic diameter
was used as an estimate of the left ventricular preload,
although this approach has limitations. Measuring the
short-axis dimensions may be difficult, as the heart may
change its relation to the transducer during insufflation
and positional changes of the patient. This problem
was noted particularly in the reverse Trendelenburg
position during carbon dioxide pneumoperitoneum; in
half of the patients who had CLC it was not possible
to obtain a reliable short-axis view. The diastolic
diameter was significantly increased in the presence of
carbon dioxide pneumoperitoneum, reflecting increased
venous return irrespective of position. Data on this
variable from previous prospective studies are conflicting.
Cunningham et al.18 and Dorsay et al.19 found no changes
in the left ventricular end-diastolic area measured by
TOE during carbon dioxide pneumoperitoneum in the
supine position, but noted a decrease after positioning
the patient head up. Zuckerman et al.13 observed a
significant reduction in left ventricular end-diastolic
volume during carbon dioxide pneumoperitoneum but no
further changes when the patient was placed in the reverse
Trendelenburg position. In contrast, Gannedahl et al.20
showed increased left ventricular volume during carbon
dioxide pneumoperitoneum, irrespective of posture, in
patients with good cardiovascular function.
Arterial pressure basically represents the afterload
opposing left ventricular ejection. In the present study
MAP was significantly higher during carbon dioxide
pneumoperitoneum than in the gasless group during
traction, in accordance with the results of Koivusalo
et al.4 . Several other observational studies have also
shown that carbon dioxide pneumoperitoneum increases
MAP3,10,19,21 . In the present study the changes were most
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British Journal of Surgery 2004; 91: 848854

Effect of pneumoperitoneum on haemodynamics and cardiac function

853

pronounced in the reverse Trendelenburg position. This


is in accordance with the results of Odeberg et al.6 and
OLeary et al.5 , who related the raised MAP to an increased
concentration of renin and aldosterone.
Afterload is the load that myocardium bears when
it contracts. The greater the afterload, the less the
myocardium contracts and shortens. Fractional shortening
therefore provides information on left ventricular function.
Fractional shortening was less during CLC than GLC
in the present study; this was most pronounced in
the reverse Trendelenburg position, suggesting reduced
cardiac performance in this position as a consequence
of the pneumoperitoneum. Irwin and Ng21 similarly
demonstrated reduced fractional area during carbon
dioxide pneumoperitoneum, using a two-dimensional
echocardiographic backscatter imaging technique. On the
other hand, Gannedahl et al.20 showed no changes in
end-systolic area or fractional area during carbon dioxide
pneumoperitoneum.
The integrated function of the cardiovascular system
is represented by the CO. Changes in CO may result
from many factors and do not merely reflect myocardial
contractility. The method of calculation of CO used in
this study has certain limitations, most notably that it
requires calculation of the sectional area. This was not
possible with 2025 per cent of the present measurements.
Furthermore, the measured diameter must be squared
in the calculation of blood flow, so any errors will
be multiplied. CO measurements should therefore be
interpreted with caution. However, as a single method was
used to evaluate heart performance in this study, changes
between and within the groups may reflect true differences.
The lack of effect of carbon dioxide pneumoperitoneum on
CO may be explained by the observed increase in heart rate.
This result is in agreement previous data10,22,23 . Several
other studies have investigated CO during laparoscopy.
Using a SwanGanz catheter in 15 patients with ASA
grade I, Joris et al.2 showed a reduction of 50 per cent in
CO during carbon dioxide pneumoperitoneum compared
with preoperative values. No additional volume loading
was given before laparoscopy, but 4 ml per kg per h
lactated Ringers solution was infused to compensate for
intraoperative losses. Hirvonen et al.24 , however, noted a
reduction in CO of less than 20 per cent when patients
were given extra volume loading before laparoscopy.
Using transoesophageal Doppler imaging, Alishahi et al.25
showed a similar reduction in CO during carbon dioxide
pneumoperitoneum and head-up tilt. The question is,
however, whether the pneumoperitoneum or other factors
are responsible for the decrease in CO. In a small,
randomized study CO was measured by means of a

SwanGanz catheter and thermodilution method in 15


patients assigned to open cholecystectomy, CLC or
GLC26 . In contrast to the present results, the cardiac
index of patients undergoing CLC was significantly
reduced by 15 per cent, whereas the heart rate remained
stable. It would therefore appear that carbon dioxide
pneumoperitoneum has little if any effect on CO in
patients with a healthy cardiovascular system, provided
that additional fluids are given.
Maximum haemodynamic changes have been observed
when carbon dioxide pneumoperitoneum is created with
the patient in reverse Trendelenburg position, with a
decline in cardiac index of 50 per cent2 . The change
from supine to the reverse Trendelenburg position may
be accompanied by a fall in venous return, reflected
by a change in left ventricular end-diastolic area18 . In
the present study, left ventricular end-diastolic diameter,
which reflects left ventricular filling, was significantly
higher immediately after creation of carbon dioxide
pneumoperitoneum than that measured beforehand and
that seen with the gasless technique. However, during
carbon dioxide pneumoperitoneum the left ventricular
end-systolic diameter was significantly higher than that in
the gasless group, resulting in reduced fractional shortening
overall and indicating reduced left ventricular performance
in the reverse Trendelenburg position immediately after
insufflation of carbon dioxide.
CLC in patients with ASA physical status I or II was
associated with significant cardiac and haemodynamic
changes, although CO was not affected as other
variables compensate for the effects of carbon dioxide
pneumoperitoneum in healthy individuals. Whether
similar changes occur in patients with cardiac disease
remains to be investigated.

Copyright 2004 British Journal of Surgery Society Ltd


Published by John Wiley & Sons Ltd

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Acknowledgements

This study was supported by funding from Nordjyllands


Amts Forskningsraad, Aalborg Stifts Julelotteri and Det
Obelske Familefond.
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British Journal of Surgery 2004; 91: 848854