D. Tsoutsos 1; A. Gravvanis 1; D. Kakagia 1,2; S. Ghali 3; A. Papalois 1
Department of Plastic Reconstructive Surgery, Athens General Hospital “G. Gennimatas”, Athens
1; Department of Plastic Surgery, Democritus University in Thrace, Alex/polis, Greece, and
2; Department of Plastic Surgery, The Royal Free Hospital, London, UK
Vyšlo v časopise:
ACTA CHIRURGIAE PLASTICAE, 51, 1, 2009, pp. 11-14
The benefits of the application of vascular
delay in restorative surgery have already been recognized and acknowledged,
though its pathophysiology is not yet fully understood (7). Vascular delay has
been clinically applied to the superior pedicled transverse rectus abdominis
musculocutaneous flap for breast reconstruction following mastectomy for
patients at high risk of complications (2, 20). Surgical methods used to induce
vascular delay vary according to individual empirical strategies and include
the selective ligation of one or both stems of the deep inferior epigastric
vessels with or without occlusion of the corresponding superficial epigastric
vessels (10, 16, 17). However, regardless of which vessels undergo ligation, it
has been customary to ligate both the artery and the corresponding vein
The inferiorly based transverse rectus
abdominis musculocutaneous flap has been widely investigated as an appropriate
experimental model for the study of vascular delay (3, 4, 8), despite the fact that
it is not directly analogous to the human equivalent (9).
attempts at selective vascular delay involving preservation of ipsilateral
venous outflow have shown no improvement over combined arterial and venous
interruption (18). In the same study, selective venous division did not result
in a significant increase in flap survival, indicating the importance of
adequate venous outflow.
hypothesized that TRAM flap survival could be improved with selective ligation
of arterial inflow with preservation of venous outflow not only in the superior
ipsilateral pedicle but also in both superior and inferior contralateral
Thirty-six Wistar rats,
16–20 weeks old, weighing 280–320 grams were used. The animals were housed in
an approved animal care center with 12 hour light cycles and provided with
standard rodent chow and water ad libitum. All animal studies were
approved by the Greek and European Community guidelines regulating animal
research (Reg No: 4221/ 31-12-2002).
anaesthesia was induced with intramuscular administration of a mixture
consisting of 13cc ketamine (Ketalar 50mg/ml), 2.5cc Midazolam (Dormicum
5mg/ml) and 1cc atropine (Atropine Sulphate 1mg/ml). The adequacy of the
anaesthesia was monitored prior to commencing surgery and at regular intervals
throughout the operative procedure by response to forepaw stimulation. If
minimal or no response was observed following firm pinching of the forepaw, then
an appropriate level of anaesthesia was judged to have been achieved. Other
parameters monitored throughout the anaesthetic and post-operatively until
recovery included respiration and skin colour / turgor. Prior to coming round
from the anaesthesia the rats received an intra-peritoneal injection of
buprenorphine 0.05 mg/kg.
Rats were randomly
assigned to one of three groups consisting of 12 animals each, differentiated
according to the type of vascular ligation selected for the first experimental
stage in order to achieve the delay phenomenon.
Group A: was used as a control group, and
no vessels were ligated.
Group B: The right inferior epigastric vessels were
preserved, while 3 arteries and 3 veins were ligated. The right deep superior
and left inferior and left superior deep vessels were ligated.
Group C: The right inferior epigastric vessels were
preserved, while 3 arteries and 1 vein were ligated. The right superior vessels
(artery and vein) as well as the left superior and inferior epigastric arteries
(veins preserved) were ligated.
the first stage of this procedure, small 1 cm horizontal skin incisions were made
to the left and right of the xiphoid process using the operating microscope for
ligation of the left and right deep superior epigastric vessels respectively
(Fig. 1). A similar incision was made in the anterior rectus sheath and
the muscle fibres spread in order to expose the superior epigastric vessels.
For ligation of the left deep inferior epigastric vessels a small 1 cm horizontal skin
incision was made in the left iliac fossa. Identification of the iliac vessels and preparation of the inferior epigastric
vessels at their point of origin was carried out, again using the operating
microscope. This was followed by ligation of the vascular pedicle (Group B) or
selective ligation of the artery (Group C) with nylon 8-0 stitches.
a delay period of 1 week (15), the second stage of the procedure was
carried out. This involved the preparation and elevation of the transverse
rectus abdominis musculocutaneous (TRAM) flap based on the right inferior
epigastric vessels. The skin paddle was of similar dimensions in all the
experimental animals (Fig. 2A). The skin paddle was elevated with careful
preservation of all musculocutaneous perforators from the right rectus
abdominis muscle. The right rectus abdominis muscle was dissected from its
origin superiorly at the right rib arc and detached from the ipsilateral
abdominal wall and from the linea alba. The preparation of the right TRAM flap
continued inferiorly to the right deep inferior epigastric vessels which were
preserved (Fig. 2B). Finally, the flap was photographed (Sony Cybershot DSCF717
5.0 megapixel digital camera) and inset in its original position with 4-0 silk.
In control group
A the musculocutaneous flap based on the right inferior epigastric vessels
did not undergo an initial surgical delay procedure. In addition, venous
patency in all group C vascular pedicles was confirmed with an Acland’s test
prior to proceeding with the second stage.
Ninety-six hours later
the animals were re-anaesthetised to evaluate skin island viability. The skin
islands were harvested and mounted onto a wooden frame. They were then
photographed (Sony Cybershot DSCF717 5.0 megapixel digital camera) and the
images analyzed using SigmaScan (SPSS, Inc., Chicago, IL) to quantify and
calculate flap survival. The area of flap survival divided by the total flap
area multiplied by 100 was used to calculate the percentage of flap survival. Results
are expressed as a mean ± standard deviation.
analysis was performed using the SigmaStat statistical program version 3.1
(SPSS Science, Chicago, IL). An analysis of variance (ANOVA) was used to
evaluate differences between the experimental and control groups. A value
of p<0.05 was considered significant. An additional post hoc test (Tukey’s
Test) was carried out to verify any pairwise differences between groups.
All animals tolerated
the surgical procedure and recovered smoothly from the anaesthesia. Table 1
illustrates the survival percentage of the flap with regard to the type of
The percentage of
survival in control group A was 50±6%;
group B showed a percentage survival of 60±4%
and group C 85±4% (see Table 1).
indicated a statistically significant difference in the survival
percentage between groups C and A, and between groups C and B (p<0.05,
occlusion of the three vascular pairs in group B improved the survival
percentage in comparison to the control group A, but not to a statistically
significant level (p>0.05, ANOVA). The selective occlusion of both the
arteries on the left (opposite the flap blood supply side) with simultaneous
preservation of the corresponding veins in group C improved the flap survival
percentage to a statistically significant degree compared to groups
A and B.
Necrosis was observed
in the control group A in zones II, III and IV (Fig. 3A). Flap necrosis
was mainly observed in group B in zone IV (left outer part of the flap,
opposite the right rectus abdominis muscle) which should theoretically have the
poorest blood supply (Fig. 3B), and it is worth noting that none of the animals
in group C exhibited necrosis in this zone (Fig. 3C).
The transverse rectus
abdominis musculocutaneous flap is one of the most commonly used flaps in
breast reconstruction following mastectomy (5). Various techniques have been
used to improve the blood supply to the flap in order to safely transfer large
skin islands. Techniques include the use of a “double pedicle” (11), based
on the superior epigastric vessels with or without simultaneous microvascular
anastomoses of the inferior epigastric vessels (1), and the use of a free
musculocutaneous flap based on the inferior epigastric vessels (19) or inferior
epigastric vessel perforators (12). In spite of advances made in this field and
increased experience in free tissue transfer, the superior epigastric vessel
pedicled island flap is often applied to patients at high risk of complications
(2). In this context, there have been a number of both experimental (3, 6,
8, 9, 15, 18) and clinical (2, 10, 16, 17, 20) attempts at applying the delay
phenomenon to the rectus abdominis flap.
The rat transverse
rectus abdominis musculocutaneous flap was the first model used to study the
delay phenomenon in 1978 (6) and is analogous in many ways to the human TRAM
flap with respect to myocutaneous perforators and dominant vs. non-dominant
pedicles. It has since proven to be a reliable and consistently
reproducible model for the study of the delay phenomenon.
The choice of
a 1-week-time interval between the delay and flap elevation in the present
study was not arbitrary but based on experimental work by Ozgentas et al. (15)
as well as the clinical work of Restifo et al. (16, 17), who provided evidence
that one week is sufficient an interval for the benefits of a delay
procedure to occur.
A number of
theories have been suggested as to the cause of the delay phenomenon (7).
McFarlane et al. (13) suggested that the delay phenomenon is based on gradual
reduction of blood supply, resulting in ischaemia, which in turn stimulates the
development of collateral blood flow. On the other hand Myers et al. (14) put
forward the assumption that the sudden increase in tissue pCO2 causes vascular dilation and an increase in the flap
blood supply. More recent interpretation of the delay phenomenon comes from
Taylor et al. (20), who suggest that after division of the dominant vascular
stem of an angiosome (e.g. the deep superior to the rectus abdominis) the choke
vessels connecting it with its neighbouring angiosome dilate, and as
a result the blood supply to this neighbouring angiosome increases.
In addition Taylor et
al. (20) have suggested that insufficient venous outflow causes the division of
the venous part of the vascular pair resulting in blood reflux into the
secondary vascular pair. On these grounds we decided to obstruct the arterial
inflow to the contralateral left rectus abdominis muscle with division of the
left superior and inferior epigastric arteries while maintaining venous outflow
by preserving the left superior and inferior veins. In other words, we achieved
arterial flow into one angiosome (right rectus) with the preservation of the
inferior epigastric artery, and we ceased the flow of the superior and inferior
epigastric arteries into the neighbouring angiosome (left rectus) while
maintaining venous outflow (superior and inferior epigastric veins).
we demonstrated that zone IV, with the poorest blood supply, exhibited no
necrosis in any group C animals. This indicates that preservation of the venous
outflow of zone IV with simultaneous reduction of its blood supply results in
increased blood supply. This conclusion is further supported by direct
comparison of group C to group B, where there was no venous outflow in zone IV.
et al. (18) demonstrated in the rat rectus abdominis muscle model that
selective ligation of the ipsilateral superior epigastric artery bears the same
results as ligation of the superior epigastric vascular pair (artery and vein).
They also demonstrated that selective ligation of the superior epigastric vein
had a detrimental effect on flap viability, since the survival percentage
in this case was no different to that of a control group where delay was
not performed. The authors did not apply any kind of delay to the angiosomes on
the contralateral side (left rectus abdominis muscle) and therefore did not
observe any remarkable improvement to zone IV. Limiting contralateral arterial
inflow while preserving contralateral venous outflow therefore appears to
preserve the ischaemia required to stimulate vascular delay while
simultaneously preventing venous congestion and therefore flap necrosis.
Further experiments are planned to address the relative contribution of each of
the contralateral venous outflow channels to flap survival.
There is no doubt that
clinical interest in the delay phenomenon applied to the rectus abdominis
muscle, mainly regarding breast reconstruction, is focused on increasing blood
supply to zone IV. Surgical delay techniques applied herein have the
disadvantage of excess surgical manipulations, but this is balanced by
increased viability of the musculocutaneous flap and especially by the
outstanding increased survival rate of zone IV. We conclude that selective
preservation of venous outflow improves TRAM Flap survival following vascular
delay and should be considered in high risk patients undergoing autologous
breast reconstruction with a pedicled musculocutaneous flap.
Kakagia, M.D, PhD., FEBOPRAS
University In Thrace
P. Kirillou Str,
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