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org

Uterine-sparing surgical procedures to control


postpartum hemorrhage
Hanane Bouchghoul, MD, PhD; Hugo Madar, MD; Benoit Resch, MD; Beth L. Pineles, MD, PhD; Aurélien Mattuizzi, MD;
Alizée Froeliger, MD; Loı̈c Sentilhes, MD, PhD

Introduction
Postpartum hemorrhage today accounts Postpartum hemorrhage remains one of the principal causes of maternal mortality in the
for 27% of maternal deaths throughout United States and throughout the world. Its management, which must be multidisci-
the world and is thus one of their leading plinary (obstetrics, midwifery, anesthesiology, interventional radiology, and nursing),
causes.1,2 At least 90% of maternal depends on the speed of both diagnosis and implementation of medical and surgical
deaths from postpartum hemorrhage are treatment to control the hemorrhage.
avoidable because they often follow a The aim of this work is to describe the various techniques of vessel ligation and of uterine
delay in diagnosis, a delay in manage- compression for controlling and treating severe hemorrhage, and to present the ad-
ment, or insufficient treatment.2 A sur- vantages and disadvantages of each.
vey has shown that, depending on the It is not difficult to perform vessel ligation of the uterine arteries: O’Leary’s bilateral
technique, 30% to 60% of attending ligation of the uterine artery, Tsirulnikov’s triple ligation, and AbdRabbo’s stepwise
obstetrician-gynecologists report that uterine devascularization (that is, stepwise triple ligation). These procedures are asso-
they have not mastered the surgical ciated with a high success rate (approximately 90%) and a low complication rate.
techniques for managing severe hemor- Bilateral ligation of the internal iliac (hypogastric) arteries is more difficult to perform and
rhage (vessel ligation and/or uterine potentially less effective (approximately 70% effectiveness) than the previously
compression sutures).3 This same survey mentioned procedures. Its complication rate is low, but the complications are most often
suggests that up to 18% of obstetricians serious. There is no evidence that future fertility or subsequent obstetrical outcomes are
have not mastered any of these impaired by ligation of either the uterine or internal iliac arteries.
methods.3 It is thus essential to dissem- There are many techniques used for uterine compression sutures, and none has shown
inate these treatments to manage severe clear superiority to another. Uterine compression suture has an effectiveness rate of
approximately 75% after failure of medical treatment and approximately 80% as a
second-line procedure after unsuccessful vessel ligation. The risk of synechiae after
From the Department of Obstetrics and
Gynecology, Bordeaux University Hospital, uterine compression suture has not yet been adequately evaluated, but is probably
Bordeaux, France (Drs Bouchghoul, Madar, around 5%.
Mattuizzi, Froeliger, and Sentilhes); Department The risk of synechiae after uterine compression suture has not yet been adequately
of Obstetrics and Gynecology, Rouen University evaluated, but probably ranges between 5% and 10%.
Hospital, Rouen, France (Dr Resch); Department
of Gynecologic Surgery, Clinique Mathilde, The methodologic quality of the studies assessing uterine-sparing surgical procedures
Rouen, France (Dr Resch); and Department of remains limited, with no comparative studies. Accordingly, no evidence suggests that any
Obstetrics, Gynecology and Reproductive one of these methods is better than any other. Accordingly, the choice of surgical
Sciences, McGovern Medical School, The technique to control hemorrhage must be guided firstly by the operator’s experience.
University of Texas Health Science Center,
Houston, TX (Dr Pineles).
If the hemorrhage continues after a first-line uterine-sparing surgical procedure and the
patient remains hemodynamically stable, a second-line procedure can be chosen.
Received March 19, 2022; revised June 5, 2022;
accepted June 12, 2022. Nonetheless, the application of these procedures must not delay the performance of a
L.S. has carried out consultancy work and been
peripartum hysterectomy in cases of hemodynamic instability.
a lecturer for Ferring Laboratories in the previous Key words: fertility, internal iliac artery ligation, obstetrical prognosis, peripartum
3 years. The other authors report no conflict of
interest.
hysterectomy, postpartum hemorrhage, uterine artery ligation, uterine compression
sutures (B-Lynch, Hayman, and Cho)
This research received no specific grant from
any funding agency in the public, commercial, or
not-for-profit sectors.
Corresponding author: Loïc Sentilhes, MD, PhD. hemorrhage through as many pathways Vessel ligation
loicsentilhes@hotmail.com as possible.3 Uterine artery ligation
0002-9378/$36.00 This study aimed to present the Bilateral uterine artery ligation.
ª 2022 Elsevier Inc. All rights reserved. uterine-sparing surgical procedures This technique was initially described by
https://doi.org/10.1016/j.ajog.2022.06.018
currently available to treat postpartum Waters4 in 1952. He reported that this
hemorrhage refractory to medical treat- ligation enabled a 90% reduction of the
ment, and their advantages and disad- blood flow to the uterus (vs only 48%
vantages (Video 1). with ligation of the internal iliac

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mean success rate for uterine artery li-


FIGURE 1
gations was 93%. Therefore, the bilateral
Bilateral ligation of the uterine arteries ligation of uterine veins and arteries is a
simple, rapid technique that is easily
reproducible. It can always be per-
formed before a hysterectomy and
functions as the initial step to limit
blood loss before peripartum hysterec-
tomy. Thus, bilateral uterine artery
ligation does not delay the performance
of a peripartum hysterectomy.
The only complication reported after
bilateral ligation of the uterine arteries is
a retroperitoneal hematoma, reported in
A, Bilateral ligation of the uterine arteries (HL), then a second lower bilateral ligation 2 to 3 cm below
2 cases (1%) in O’Leary’s series.7 Only 15
the first (LL). B, Intraoperative view. Stepwise ligation of the uterine pedicle from the right side: uterus
pregnancies have been reported after
gently retracted superiorly and contralaterally by the assistant surgeon, the RL transected, and the
ligation of only the uterine arteries.7,9,10
bladder pushed away by the retractor. A PW is opened. Then, working from back to front, largely on
All proceeded with no complications
the myometrium, a HL is performed and then a LL of the uterine pedicle.
and led to term births of healthy
bl, bladder; HL, high ligation; LL, low ligation; o, ovary; PW, peritoneal window; RL, round ligament; ur, ureter; ut, uterus.
children.10
Bouchghoul. Uterine-sparing surgical procedures. Am J Obstet Gynecol 2022.
Tsirulnikov’s triple ligation.
This technique is a variant of bilateral
uterine artery ligation, known as ligation of
the uterine vessels, first described in
arteries).4 Performed transabdominally, Passing the suture from posterior to 1974.11 It systematically combines bilateral
it involves ligating the ascending anterior may decrease the risk of bowel ligation of both the round and the utero-
branches of the uterine arteries together injury.5 ovarian ligaments with bilateral uterine
with the deep venous plexus that ac- A second ligation called a low or artery ligation (Figure 2 and Video 2).
companies them. This ligation can be stepwise ligation can be performed 2 to During pregnancy, uteroplacental
performed in stages for each pedicle. The 3 cm below the preceding ligation to perfusion comes mostly from the uterine
technique begins by the exteriorization occlude the branches feeding the cervix arteries. Nonetheless, in 4% of cases, it is
of the uterus, pulling it gently upward (Figure 1). Because a single ligation instead the ovarian arteries that supply
and contralaterally to distance it from presents the risk of incomplete occlu- most of the placenta’s perfusion. Perfu-
the ipsilateral ureter; a self-retaining sion of the uterine artery (provided sion by the round ligament artery is
retractor is then placed. The ligation is below), we recommend performing the anecdotal.12 The ligation and transection
prepared by making an incision in the second one systematically.5 Later on in of the round ligament improves access to
vesicouterine peritoneum and dissecting the procedure, after the ligation, the the uterine pedicle without later func-
the bladder from the uterus 3 to 4 cm absence of a pulse in the uterine pedicle tional repercussions. Moreover, ligation
below the hysterotomy, if the delivery must be verified. It is important to insist of the round ligament arteries and the
was cesarean. The bladder is protected by on the need for sustained traction of the utero-ovarian ligaments may prevent the
the placement of a bladder blade. The uterus and the importance of fenestra- resumption of uterine perfusion by
round ligament can then be ligated and tion of the broad ligament to keep the various collateral networks (right/left
transected to separate the anterior and ureter out of the way. The depth into the transverse anastomoses between
posterior leaves of the broad ligament myometrium must be significant to branches of the uterine arteries; infra-
and facilitate safe access to the uterine avoid injuring the uterine vessels, which tubal and subovarian arcades formed by
pedicle. A finger is used to identify the could cause an arteriovenous fistula, but the anastomoses of the terminal
uterine artery and electrocautery used to penetrating the uterine cavity must be branches of the tubal and ovarian ar-
open the avascular zone of the anterior avoided.6 O’Leary7 reported his experi- teries; a branch of the round ligament
and then posterior leaf of the broad lig- ence ligating uterine arteries in a retro- born of the uterine artery anastomosed
ament 3 to 4 cm (more experienced spective study of 265 cases over a 30- to the round ligament artery).12 In the
surgeons can perform this procedure year period, with a success rate of article describing this technique, Tsir-
without sectioning the round ligament, 97%. In interpreting this exceptional ulnikov11 reported 24 cases, all because
but with a narrower window opening). rate, it must be noted that this series of uterine atony, treated by triple ligation
The ligation is performed with absorb- does not include any ligations for with a 100% success rate. A French study
able suture, through the myometrium, 2 placenta accreta spectrum.7 In the liter- retrospectively aimed at assessing the
to 3 cm below the incision (Figure 1). ature review by Doumouchtsis et al,8 the effectiveness of Tsirulnikov’s triple

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artery and that the surgeon cannot di-


FIGURE 2 FIGURE 3
agnose even after verifying the absence of
Tsirulnikov’s triple ligation11 Stepwise uterine a pulse at the uterine pedicle later during
devascularization14 the procedure.5 The persisting patency of
the uterine artery (assessed by arteriog-
raphy in cases of persistent hemorrhage
after uterine artery ligation5) can cause
the procedure to fail to stop the hemor-
rhage. Moreover, unlike ligation of the
uterine arteries at a single point, the
stepwise ligation devascularizes both the
lower uterine segment and the upper
cervix. It is thus appropriate for dealing
with disorders of the lower uterine
segment.
AbdRabbo reported a series of 103
Ligation of: (1) uterine arteries, (2) the round women and a success rate of 100%.14
AbdRabbo has proposed a stepwise uterine
ligament, and (3) the utero-ovarian ligaments. The bilateral double ligation of the
devascularization in 5 steps, with each step
bl, bladder; o, ovary; ur, ureter; ut, uterus. uterine arteries (steps 1e3) brought the
being performed only if the preceding step did
Bouchghoul. Uterine-sparing surgical procedures. Am J hemorrhage under control for 96 of
Obstet Gynecol 2022. not stop the hemorrhage within 10 minutes:
unilateral and then bilateral ligation of the these 103 (93%) women: 65 of 66 (98%)
uterine arteries (1þ2), stepwise low ligation of of those with uterine atony, 15 of 17
both uterine arteries (3), unilateral and then (88%) with placental abruption, all 5
ligation. Among the 56 women who had bilateral ligation of the suspensory ligaments of (100%) with placenta previa, and both of
Tsirulnikov’s triple ligation as a first-line the ovary (4þ5). We advised against steps 4 the women (100%) with placenta accreta
treatment, 77% (43/56) subsequently and 5 because of the risk of subsequent ovarian spectrum disorders.14 Steps 4 and 5 were
required a second uterine-sparing sur- failure. necessary only in all 4 (100%) women
gical procedure.13 To explain the differ- bl, bladder; o, ovary; ur, ureter; ut, uterus. with afibrinogenemia (n¼4) and 6 of 9
ence in success rate from that reported Bouchghoul. Uterine-sparing surgical procedures. Am J (67%) women with a Couvelaire
by Tsirulnikov,11 O’Leary,7 and others,10 Obstet Gynecol 2022. uterus.14
the authors suggested that some sec- We evaluated AbdRabbo’s stepwise
ondary procedures may have been uterine devascularization with a success
performed unnecessarily.13 They under- after dissection of the bladder from the rate of 72% (16/58),10 less than that
lined that a second uterine-sparing sur- uterus, (4) unilateral ligation of an reported by AbdRabbo14 and by au-
gical procedure was less likely to be ovarian pedicle, and (5) ligation of the thors who performed bilateral double
performed over time, and considered contralateral ovarian pedicle (Figure 3). ligation of the uterine arteries and no
that this may reflect a learning period In the initial publications, the author other vessels.7,9,15 AbdRabbo also re-
necessary for the surgeons to feel confi- used the term “ovarian vessel ligation” to ported the medium and long-term
dent with Tsirulnikov’s triple ligation.13 describe steps 4 and 5.14 The term is maternal outcome for 45 of the 103
Stepwise uterine devascularization. confusing because it could designate the women with stepwise uterine devascu-
AbdRabbo et al described this technique ligation of either the utero-ovarian liga- larization for postpartum hemor-
in 1994.14 The principle of this stepwise ment (the stepwise ligation would thus rhage,14 noting that they observed no
ligation method is the progressive be a stepwise triple ligation with a double modification of the rhythm, volume, or
devascularization of vessels supply ligation of each uterine artery) or of the duration of their menstrual cycles.
ing the uterus. Each step is performed suspensory ligaments of the ovary. Given Among the 15 women who stopped
only if the preceding step did not stop that AbdRabbo used the term “ovarian contraception, 11 became pregnant af-
the hemorrhage within 10 vessels” several times, it is probable that ter a mean time to conception of <1
minutes (Video 2). This technique he was referring to the latter.14 year, and all gave birth at term to
therefore comprises the following 5 The advantage of this technique is its healthy children.14 These pregnancies
successive steps: (1) unilateral ligation of explicit recommendation of a double were obtained both in women who had
the ascending branch of a uterine artery, ligation of each uterine artery: the first 1 undergone ligation of the ovarian
as described above, (2) ligation of the cm below the hysterotomy (after a ce- pedicle (n¼5) and those who had not
contralateral uterine artery, (3) lower sarean delivery) and the second 3 cm (n¼6). Nonetheless, AbdRabbo re-
ligation of both uterine arteries and of below the first ligation. This reduces the ported no information about the 4
their cervicovaginal branches 2 cm risk of an ineffective ligation that does women who stopped contraception and
below the preceding upper ligations, not or only partially blocks the uterine did not become pregnant.

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We reported the follow-up of 32 Bilateral ligation of the internal iliac vessels supplying the uterus.18 The
women who underwent stepwise (hypogastric) arteries (Video 3) effectiveness of internal iliac artery
devascularization that enabled them to Bilateral ligation of the internal iliac ar- ligation seems worse than initially
avoid a hysterectomy: 9 women had teries in the management of postpartum supposed.19 Doumouchtsis et al have
only a double bilateral ligation of the hemorrhage was first described in reviewed the literature about its effec-
uterine arteries, 11 women a double 189817 and was considered the reference tiveness,8 which varies among authors
bilateral ligation of the uterine arteries technique for many years (Video 3). from 39% to 100%, with a mean suc-
followed by bilateral ligation of the Performed transabdominally, this tech- cess rate of 69% (136/197).8 Nonethe-
utero-ovarian ligaments, and 12 women nique can be summarized by the less, one study of 84 women reported a
a double bilateral ligation of the uterine following steps. The uterus is exterior- success rate <60%, although all liga-
arteries followed by a bilateral ligation ized and pulled gently forward and tions were performed by experienced
of the suspensory ligaments of the contralaterally, and then a retractor, self- surgeons specialized in gynecologic
ovary.10 Only 4 reported modification retaining or handheld, is placed. An oncology.20
of their menstrual cycles: 3 had post- incision is made in the posterior peri- Ligation of the internal iliac arteries
partum amenorrhea, with 2 owing to toneum at the level of the common iliac seems to be interesting principally for
ovarian insufficiency and the third artery and extended 5 to 6 cm inferiorly. the management of obstetrical injuries
owing to synechiae, whereas the fourth At the level of the sacral promontory, the such as cervicovaginal injuries and
had a necrotic and infected uterus iliac bifurcation can be palpated. On the vaginal or pelvic thrombi and for
requiring a hysterectomy at 7 months left, exposure of the iliac vessels is facil- persistent bleeding after peripartum
postpartum. All 4 had had a bilateral itated by mobilization of the sigmoid hysterectomy.21 However, it is a diffi-
ligation of the suspensory ligaments of colon and detachment of the colon, cult procedure, performed only rarely,
the ovary. Among the 16 women with peritoneum, and Toldt fascia. Dissection generally in major emergencies, and
preserved fertility who stopped their of the peritoneum continues to the involving a surgical field rarely
contraception, no secondary infertility bifurcation of the internal and external dissected by obstetrician-gynecologists
was observed.10 Twelve women had 16 iliac arteries. Because the ureter passes who do not practice oncologic sur-
pregnancies: 1 ectopic pregnancy, 2 directly under this bifurcation, it must gery. It can cause severe morbidity:
elective abortions, and 13 term de- be identified and moved safely out of the iliac vein injury, ligation of the ureter
liveries of 13 healthy children. These way. This avoids a ureteral injury and or iliac artery, gluteal claudication, and
pregnancies occurred both among exposes the surgical field. The internal peripheral vein injuries.8 If performed
women who had undergone ligation of iliac artery is then dissected at a distance well, it may be difficult to perform a
the suspensory ligaments of the ovaries from the surrounding structures. Liga- secondary embolization should the
(n¼5) and among those who had not tion of the internal iliac artery involves ligation fail.5,22 Sanders et al23 recently
(n¼7). The postpartum hemorrhage its circumferential dissection to allow described a simplified approach to oc-
recurrence rate in this series was 31%, the passage of a right-angle forceps for clusion of the internal iliac artery,
similar to that observed after bilateral suture ligation. A right-angle forceps is limiting retroperitoneal dissection by
ligation of the internal iliac arteries.10,16 introduced just under the artery, creating a space only on each side of
In conclusion, the single or double perpendicular to the vessel, with a pas- the artery, using a forceps placed lateral
bilateral ligation of the uterine arteries, sage from the outside to the inside to and parallel to the artery. A clip applier
whether or not followed by bilateral avoid damaging the underlying vein. can be easily moved through the nar-
ligation of the utero-ovarian ligaments, The ligation is performed 2 cm below row space created on both sides of the
does not seem to impair women’s fertility the iliac bifurcation to avoid ligating the artery and can occlude the artery with
or their subsequent obstetrical posterior branches feeding the gluteus. A 2 titanium vascular clips. This
outcome.10 This technique is simple, nonabsorbable suture is then inserted approach is simpler and faster than the
rapid, and easily reproducible. It can al- into the open right-angle forceps and technique initially described. The au-
ways be performed before a hysterec- passed around the artery. The absence of thors have not reported any complica-
tomy, especially because it constitutes the a pulse in the uterine pedicle can be tion in their series of 32 cesarean
first surgical steps of this more drastic verified after the ligation to confirm, in hysterectomies with clips placed by this
procedure. Conversely, double bilateral case of doubt, that it was not the external technique to occlude the internal iliac
ligation of the uterine arteries associated iliac artery that was ligated (Video 3). arteries.23 Invasive placentation was the
with bilateral ligation of the suspensory This ligation must systematically be indication for the cesarean hysterec-
ligaments of the ovaries seems to impair performed bilaterally. That is, a uni- tomies in this series.23
fertility (in 30% of our cases: 4/12) and lateral ligation can be a source of fail- In any case, ligation of the internal
lead to ovarian insufficiency (2/12). ure because of the existence of iliac arteries requires thorough knowl-
Ligation of these ligaments should numerous collateral networks between edge of the pelvic vascular anatomy and
therefore not be performed.10 the internal iliac artery and other adequate exposure.

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What technique of vessel ligation anterior and posterior walls together to Uterine compression sutures: the Cho
should you choose? exert pressure on it and prevent it from procedure
There are currently no studies, either filling up with blood. The objective of this procedure is to
prospective or retrospective, that have induce hemostasis by compression by
compared efficacy and morbidity be- Uterine compression suture: the applying either multiple simple trans-
tween ligation of the uterine arteries and B-Lynch suture (Video 4) fixion sutures29,30 or multistitch square
ligation of the internal iliac arteries. The In 1997, B-Lynch was the first author to sutures between the anterior and poste-
urgent nature of postpartum hemor- describe a technique of uterine rior uterine walls (Figure 5).31 In 2000,
rhage makes the feasibility of controlled compression suture, which he used to Cho et al31 were the first to describe a
trials, randomized or not, difficult. In the control postpartum hemorrhage in 5 multistitch suture technique in squares
absence of any type of controlled study, women.26 This technique involves that they termed “hemostatic multiple
no professional society has recom- creating a mediolateral suture as a brace square suturing.” This technique in-
mended performing one of these first- around the uterine body aimed at volves identifying an area of heavy
line treatments over another. The ques- bringing the anterior and posterior bleeding and suturing the serosa of the
tion is still widely debated in the litera- uterine walls together to compress the anterior wall to the serosa of the poste-
ture, and the place of these different uterus (Figure 4 and Video 4). An open rior wall by stitches forming a square
techniques continues to depend on the uterine incision was necessary for the (Figure 5). This square suture requires
culture of the country and even of each initial version of this technique.26 the placement of 4 suture points by a
center.24 Accordingly, the choice must be Nonetheless, because hemorrhage straight needle mounted with No. 0 pol-
guided firstly by the operator’s experi- resistant to medical treatment (utero- yglactin 910 (Figure 5). The procedure is
ence. Nonetheless, the ligation of uterine tonics) is almost always diagnosed after repeated as many times as necessary.
arteries compared with that of the in- the hysterotomy has been sutured, this The principal indication for uterine
ternal iliac arteries seems easier to learn mediolateral brace suture can be per- compression suture techniques is uterine
and perform and is associated with fewer formed after the incision has been atony. It seems especially useful for the
adverse events.3,25 A national survey us- closed. It is therefore unnecessary to diffuse bleeding that occurs in the lower
ing questionnaires completed anony- reopen the incision or—if delivery was uterine segment. Since its initial
mously by 286 attending obstetrician- vaginal—make a new incision.27 B- description as a series of 23 cases, this
gynecologists in France showed that Lynch initially used No. 2 chromic technique has, like the B-Lynch method,
33% of these specialists considered that catgut suture, but most recently rec- spread widely throughout the world. It is
they had not mastered bilateral ligation ommends using a No. 1 polyglecaprone very probably the most frequently used
of the uterine arteries, whereas 40% had 25 monofilament, mounted to a 70- uterine compression suture technique
not mastered Tsirulnikov’s triple liga- mm semicircular hand needle, which presently.
tion, and 62% did not feel adequately has an absorption profile that decreases
skilled in ligation of the internal iliac with time: from 60% at 7 days to 20% Uterine compression suture variants
arteries.3 The numbers were much at 14 days, with resorption complete Hayman et al modified B-Lynch’s initial
higher when the same questions were between 90 and 120 days (code W3709, technique by substituting for the single
asked to residents in obstetrics- information available at tcb@fsmail. suture 2 independent mediolateral ver-
gynecology legally authorized to cover assets).28 This procedure can be per- tical braces that can be positioned
call duties alone.25 Specifically, among formed with a large round needle if a without the need for a hysterotomy
the residents, 74% (115/156) did not hand needle is not available. incision (Supplemental Figure 1).32 Both
consider that they had mastered Although it has never been demon- the B-Lynch et al,26 and Hayman et al32
adequately or even at all the technique for strated formally, B-Lynch considers techniques use transfixion stitches, that
bilateral uterine artery ligation, whereas that this suture is likely to reduce the is, they go all the way through the uterine
85% (132/156) felt that way about Tsir- risk of postpartum uterine necrosis, cavity. Pereira et al33 proposed another
ulnikov’s triple ligation, and 95% (148/ pyometra, or synechiae compared with uterine compression technique using 3
156) about internal iliac artery ligation.25 polyglactin 910 suture.28 However, ac- transverse (horizontal) sutures and then
It is thus essential to disseminate these cording to B-Lynch, before any surgi- 2 longitudinal sutures applied with a No.
surgical techniques for the management cal procedure, bimanual compression 0 or 1 polyglactin 910 suture
of severe postpartum hemorrhage in as of the uterus acting on the hemorrhage (Supplemental Figure 2). The first
many ways as possible. may predict the subsequent effective- transverse suture passes through the
ness of this technique,26 although this upper broad ligaments bilaterally, in the
Uterine compression sutures too has not been demonstrated. Since avascular section (just below the uterine
These techniques of uterine compres- then, numerous variants of uterine horns); the next transverse suture is
sion have in common the performance compression sutures have been lower, and the third in the lower
of a plication of the uterus by bringing its described. segment; they thus separate the uterus

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compression based on B-Lynch’s prin-


FIGURE 4
ciples (brace) and can be performed with
B-Lynch’s technique of uterine compression by plication26 the incision closed (Supplemental
Figure 4). Other variants have been
described.30,35 Huissoud et al35 reported
a technique of uterine compression
(named “total uterine ligation”) that
does not involve transfixion of the uterus
but is based solely on 4 transverse braces,
with no longitudinal brace. It can be
considered a variant of Pereira because
the brace compresses both the uterus
and its lower uterine segment but also
the vessels feeding the uterus (uterine
arteries, ovarian arteries, and round lig-
A, Diagram. The technique described here begins on the left side: aments). Compression suturing accord-
ing to Ouahba et al uses 4 simple stitches
- The needle crosses the anterior wall of the uterus approximately 3 cm under the still open, that completely transfix the anterior and
unsutured incision to 3 cm from the left lateral edge of the left uterus. posterior walls of the uterus
- It goes back through the anterior wall of the uterus and emerges 3 cm above the incision, still (Supplemental Figure 5).30
approximately 3 cm from the left lateral edge of the uterus. Steps (1) and (2) describe the first Regardless of the technique used
“passage” of the needle. (original or modified B-Lynch et al,26
- The suture travels up the anterior wall of the uterus, crosses the top of the fundus, and descends Hayman et al,32 or Pereira et al33), to
down the left posterolateral wall. obtain the best possible uterine
- The needle pierces the posterior wall and enters the uterine cavity at the same level of the compression (and therefore possibly the
preceding suture point (3 cm above the incision), that is, in the superior portion of the uterine best outcome), it is important for the
body-isthmus junction, always approximately 3 cm from the left lateral edge of the uterus. surgical assistant to perform bimanual
- The needle again pierces the posterior wall at the same horizontal level as the previous suture compression of the uterus to reduce its
point, but this time, at approximately 3 cm from the right lateral edge (the other side) of the uterus. volume before tightening its sutures (or
Steps (4) and (5) describe the second passage of the needle. braces).27,28
- The suture, now on the posterior wall of the uterus, moves up toward the uterine fundus along the
right lateral edge of the uterus, to descend down the right anterolateral wall. Effectiveness and complications of
- It returns back through the anterior wall of the uterus and emerges 3 cm above the incision, still uterine compression techniques
approximately 3 cm from the right lateral edge of the uterus. In the literature review by Dou-
- The needle again crosses the anterior wall of the uterus, this time approximately 3 cm above the mouchtsis et al,8 the overall effectiveness
(still unsutured) incision. Steps (7) and (8) describe the third passage of the needle. rate of these different techniques was
- The incision is then sutured according to the usual technique. 92% (99/108). Important reservations
- Both ends of the suture (straight needle, No. 0 polyglactin 910) are then put under tension, helped are nonetheless necessary because this
by the assistant’s manual compression, to be able to press one wall against the other. Both literature review compiled different
sutures are then tied at a lower level of the lower segment, under the now sutured incision. techniques that differ quite substantially
from one another (B-Lynch, Cho, and
B, Intraoperative view of myometrial brace compression by B-Lynch Pereira), with studies including small
Bouchghoul. Uterine-sparing surgical procedures. Am J Obstet Gynecol 2022. numbers of individuals, heterogeneous
series (variously associated with vessel
ligation), and especially very little detail
into transverse sections. Next, the 2 technique therefore uses no transfixion about the causes and severity of the
longitudinal sutures correspond to stitches through the uterus.33 hemorrhages requiring the procedure.36
Hayman’s 2 vertical mediolateral braces Another variant of the Hayman et al In particular, although some authors
(Supplemental Figure 2).33 These longi- compression suture does not double the have reported that the B-Lynch proced-
tudinal sutures compress the uterus 2 independent braces (Supplemental ure is effective for uterine ruptures37 or
longitudinally. At the level of the lower Figure 3) and thus reduces the number placenta accreta spectrum disorders,38,39
uterine segment, they are attached to the of the transfixion passages from 4 to 2, it seems that these techniques are used in
lowest transverse suture by a simple knot which could be an advantage. Finally, the the great majority of cases solely for
that is reinforced in the back and front uterine compression according to Bhal uterine atony resistant to medical
(frontally and posteriorly). Pereira’s et al34 presents the advantage of a uterine treatment.36

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small.26,31e33 In this study, the effec- A French study aimed at assessing the
FIGURE 5
tiveness rate was 75% (95% confidence effectiveness of uterine compression su-
Technique of hemostatic multiple interval [CI], 69e81), and the hysterec- ture after the failure of a Tsirulnikov
square suturing by Cho et al31 tomy rate did not differ by type of triple ligation. Second-line treatment by
uterine compression used (B-Lynch, uterine compression had a success rate of
B-Lynch variant, compression sutures, 88% (5/43).13 Another study assessed
or multiple sutures).40 the effectiveness of ligation of the inter-
A French survey used an anonymous nal iliac arteries, either alone or in
questionnaire completed by 286 combination with other uterine-sparing
obstetrician-gynecologists who had procedures. Of the 26 women with
completed their residencies, and showed hemorrhage owing to uterine atony,
that 37% of these specialists did not feel 31% (8/26) of women had ligation of the
that they had mastered the use of uterine internal iliac arteries after a first-line B-
compression sutures; 47% felt that way Lynch uterine compression failed, and its
about peripartum hysterectomies.3 The success rate was 87% (7/8).45
numbers were much higher when the These studies suggest that it is
same question was asked to residents in indeed appropriate to offer second-line
obstetrics-gynecology authorized to surgical treatment after vascular liga-
cover call duties alone.25 Among them, tion or uterine compression sutures fail
Suturing the serosa of the anterior wall to the 79% did not consider that they had to stop the hemorrhage before per-
serosa of the posterior wall in square 4-stitch mastered uterine compression sutures forming a peripartum hysterectomy
sutures. and 78% felt that way about peripartum when the woman is hemodynamically
Making this multistitch square suture requires hysterectomy.25 stable.13,27,45
the placement of 4 suture points by a straight In 2014, Doumouchtsis et al41 pub- In the prospective UK study of 211
needle with No. 0 polyglactin 910: lished a systematic review of the litera- women who had uterine compression
ture including 125 women who had been sutures to treat postpartum hemorrhage,
- The first stitch (1) penetrates the anterior and treated for postpartum hemorrhage by a 13% (28/211) had a second-line treat-
then the posterior wall of the uterus. uterine compression technique. They ment by vessel ligation or uterine artery
- The second stitch (2) retransfixes the poste- estimated that 91% of the women had embolization.40 Although this study
rior wall to the anterior wall on the same resumed normal menstrual cycles by 6 does not assess the effectiveness of 2
horizontal line 2 to 3 cm from the first suture months after their uterine compression successive uterine-sparing procedures, it
point to its left. procedure and that 75% of those who shows that this approach, although
- The third (3) is performed by penetrating the wanted another pregnancy had had a live infrequent, is not rare.
anterior then posterior walls of the uterus, birth (21/28 women).
along the same vertical line 2 to 3 cm away The risk of synechiae after uterine What procedure should be used as
from and below the second suture point. compression has not yet been adequately the first-line treatment: uterine
- The fourth stitch (4) penetrates first the evaluated, but I probably around compression suture or vessel
posterior and then the anterior wall on the 5%.36,41e44 If another pregnancy is ligation?
same horizontal line at 2 to 3 cm from the desired and if oligo-amenorrhea con- No prospective or retrospective study has
third suture point, but toward the first point, tinues in the postpartum period, hys- compared effectiveness and morbidity
that is, to the right of the third suture point, teroscopy is advised to assess for between uterine compression and vessel
thus forming a square. synechiae. ligation. In a prospective series, again
- Finally, both suture ends, from points 1 and 4 from the United Kingdom (UKOSS reg-
are tied together to make a square. Is it appropriate to perform a second- ister), including 199 uterine compression
Bouchghoul. Uterine-sparing surgical procedures. Am J line uterine-sparing surgical procedures and 20 vessel ligations, the
Obstet Gynecol 2022.
procedure if the first one fails? hysterectomy rate was higher in the liga-
Few studies have assessed the effective- tion group (64%; 95% CI, 35e87 vs 25%;
ness of a second-line uterine-sparing 95% CI, 19e33).40 The very low success
surgical procedure. One study evaluated rate of vessel ligation found in this study is
The efficacy of uterine compression the effectiveness of B-Lynch sutures in 15 striking. It is probably owing to the exis-
has actually been known only since 2011 women with hemorrhage persisting tence of bias in this uncontrolled pro-
through a large prospective series of 211 despite vessel ligation.27 It showed that spective study: the small number of vessel
uterine compressions performed in the the B-Lynch sutures controlled the ligations (n¼20) compared with the
United Kingdom (UK Obstetric Sur- hemorrhage, and thus immediate hys- number of uterine compressions
veillance System [UKOSS] register)40 terectomy was avoided in 80% (12/15) of (n¼199) strongly suggests an indication
because previous studies were the cases.27 bias. This was confirmed on reading the

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Expert Review ajog.org

The place of these different techniques possible biases mentioned above make
FIGURE 6
continues to depend on the culture of this a clearly invalid comparison.
A proposed algorithm of surgical each country and even each center.24 Instead, the choice is essentially guided
technique to control postpartum Accordingly, the choice of surgical by the existence, admittedly in the form
hemorrhage refractory to technique to control hemorrhage must of case reports, of synechiae,27,42 pyo-
medical treatment be guided firstly by the operator’s expe- metra,49 and uterine necrosis,28,49 which
rience. Nonetheless, given that ligation may impair fertility after uterine
of the internal iliac arteries is probably compression, whereas these types of
the technique most difficult to mas- complications have not been reported
ter,3,25 especially for obstetrician- after uterine artery ligation.
gynecologists who do not practice sur-
gery regularly, and given that it is also Conclusion
associated with rare but possibly severe Postpartum hemorrhage remains one of
complications, we reserve this proced- the principal causes of maternal mor-
ure, if necessary, only for use after the tality in the United States and
failure of a uterine ligation and/or uter- throughout the world. Its management
ine compression (Figure 6). must be multidisciplinary (anes-
The techniques for uterine artery thesiologists, obstetrician-gynecologists,
The superscript letter a denotes this is only a ligation and those for uterine compres- interventional radiologists, midwives,
proposal. The choice, in particular for the first sion have 3 important advantages: they and nurses). The keys to its manage-
uterine-sparing surgical procedure, between are easy to perform, easy to learn,3,25 and ment lie in the speed of both diagnosis
uterine artery ligation and uterine compression associated with very low rates of imme- and the implementation of medical and
sutures depends mainly on the operator’s diate morbidity.7e9,26,27,30,31,33,47 It has surgical treatment for controlling the
preference. The superscript letter b denotes been shown that as a first-line treatment, hemorrhage, including uterine-sparing
uterine artery ligation or Tsirulnikov’s triple obstetricians prefer vessel ligation surgical procedures when medical
ligation or stepwise uterine devascularization. involving uterine arteries (51%) or treatment fails. The techniques of
The superscript letter c denotes B-Lynch or Cho uterine compression sutures (36%) to uterine artery ligation and those of
suturing techniques. internal iliac artery ligation (12%).3 The uterine compression both present the
Bouchghoul. Uterine-sparing surgical procedures. Am J learning curves for the first 2 are signif- same advantages: they are easy to
Obstet Gynecol 2022.
icantly faster than that for the latter.3 perform, easy to learn, and associated
Obstetricians considered that they had with very low rates of immediate
mastered the techniques of uterine ar- morbidity,3,25 whereas ligation of the
records; vessel ligation tended to be per- tery ligation or uterine compression after internal iliac arteries is harder to learn,
formed in the most serious and most 4 or 5 procedures, whereas it took them 9 harder to perform, and associated with
complex clinical situations.40 procedures to master internal iliac artery a low rate of complications that can,
In patients who are hemodynami- ligation.3 Accordingly, uterine artery however, be severe.3,25 Vessel ligation
cally unstable, peripartum hysterec- ligation and/or uterine compression can involving either or both of the uterine
tomy must be seriously considered. both be used as first- or second-line and internal iliac arteries does not seem
However, this intervention is associ- treatments when bleeding persists, to have any later effect on women’s
ated with considerable maternal depending on the procedure chosen fertility or their obstetrical outcomes,
morbidity.46 For this reason, it is first.27 For example, uterine artery liga- whereas complications impairing
appropriate to perform bilateral liga- tion and then uterine compression su- fertility (such as uterine necrosis, pyo-
tion of the uterine arteries (the first ture if the first fails, or uterine metra, and synechiae) have been
step of a peripartum hysterectomy) or compression suture and then uterine described after uterine compression.
uterine compression (procedures that artery ligation if the compression fails. The use of >1 uterine-sparing surgical
are most often easy and fast) to avoid Nonetheless, between the techniques of procedure is possible when the hemo-
the morbidity associated with peri- uterine artery ligation alone and those of dynamics remain stable. The choice
partum hysterectomy and/or to reduce uterine compression, we (unlike some must be guided mainly by the opera-
the volume of blood loss. other authors26,30,48) prefer uterine tor’s experience, but the techniques
It is appropriate to offer a patient who ligation as a first-line treatment must all be regularly taught, given some
is hemodynamically stable, young, pri- (Figure 6). This choice is not based on a concerning surveys suggesting that up
miparous, and/or wants subsequent belief that the effectiveness of vessel to 18% of obstetricians have not
pregnancies a first uterine-sparing sur- ligation involving the uterine arteries mastered any of the techniques.3
gical procedure, and even a second and (approximately 90%) is significantly Moreover, 37% to 62% of attending
possibly a third one before a peripartum greater than that of uterine compression obstetricians do not feel that they have
hysterectomy. (approximately 75%) because the mastered them sufficiently.

8 American Journal of Obstetrics & Gynecology MONTH 2022


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Nonetheless, it is important to recall J Gynecol Obstet Biol Reprod (Paris) 1979;8: cases reported. Br J Obstet Gynaecol
that the primary purpose of the treat- 751–3. 1997;104:372–5.
12. Pelage JP, Dref O Le, Soyer P, et al. [Man- 27. Sentilhes L, Gromez A, Razzouk K,
ment of severe hemorrhage is to save the agement of severe post-partum hemorrhage Resch B, Verspyck E, Marpeau L. B-Lynch su-
patient’s life. If possible, this should be using selective arterial embolization]. J Gynecol ture for massive persistent postpartum hemor-
done by the least invasive and least Obstet Biol Reprod (Paris) 1999;28:55–61. rhage following stepwise uterine
morbid procedure, but this objective 13. Blanc J, Courbiere B, Desbriere R, et al. devascularization. Acta Obstet Gynecol Scand
must always remain in the foreground. Uterine-sparing surgical management of post- 2008;87:1020–6.
partum hemorrhage: is it always effective? Arch 28. Price N, Lynch CB. Uterine necrosis
Accordingly, the performance of a Gynecol Obstet 2012;285:925–30. following B-Lynch suture for primary postpartum
uterine-sparing surgical procedure must 14. AbdRabbo SA. Stepwise uterine devascu- haemorrhage. BJOG 2006;113:1341.
in no case delay the performance of a larization: a novel technique for management of 29. Cristalli B, Levardon M, Izard V, Cayol A.
peripartum hysterectomy in women uncontrolled postpartum hemorrhage with [Padding of the uterine wall in severe obstetrical
preservation of the uterus. Am J Obstet Gynecol hemorrhage]. J Gynecol Obstet Biol Reprod
with hemodynamic instability. -
1994;171:694–700. (Paris) 1991;20:851–4.
15. O’Leary JL, O’Leary JA. Uterine artery ligation 30. Ouahba J, Piketty M, Huel C, et al. Uter-
ACKNOWLEDGMENTS in the control of intractable postpartum ine compression sutures for postpartum
hemorrhage. Am J Obstet Gynecol 1966;94: bleeding with uterine atony. BJOG 2007;114:
We thank Joann Cahn, for her help in editing this 920–4. 619–22.
manuscript. The authors thank the patients who 16. Nizard J, Barrinque L, Frydman R, 31. Cho JH, Jun HS, Lee CN. Hemostatic su-
kindly gave written permission for their pictures Fernandez H. Fertility and pregnancy outcomes turing technique for uterine bleeding during ce-
to be reported. following hypogastric artery ligation for severe sarean delivery. Obstet Gynecol 2000;96:
post-partum haemorrhage. Hum Reprod 129–31.
2003;18:844–8. 32. Hayman RG, Arulkumaran S, Steer PJ.
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Verspyck E, Marpeau L. Predictors of failed ligations, emergency peripartum hysterectomy 36. Sentilhes L, Gromez A, Descamps P,
pelvic arterial embolization for severe post- or arterial embolization?]. Gynecol Obstet Fertil Marpeau L. Why stepwise uterine devasculari-
partum hemorrhage. Obstet Gynecol 2009;113: 2004;32:320–9. zation should be the first-line conservative sur-
992–9. 22. Zanati J, Resch B, Roman H, et al. Buttock gical treatment to control severe postpartum
6. Howard LR. Iatrogenic arteriovenous sinus of necrosis after subtotal hysterectomy, bilateral hemorrhage? Acta Obstet Gynecol Scand
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Obstet Gynecol 1968;31:255–7. zation for control of severe post-partum hae- 37. El Daief SG, Kirwan J. The B-Lynch suture at
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Arulkumaran S. Systematic review of conserva- simplified approach. Am J Obstet Gynecol control bleeding from placenta praevia or
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devascularization for severe postpartum and gynecology. BMC Pregnancy Childbirth Uterine compression sutures for the manage-
haemorrhage. Hum Reprod 2008;23: 2019;19:91. ment of severe postpartum hemorrhage. Obstet
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11. Tsirulnikov MS. Ligation of the uterine ves- Cowen MJ. The B-Lynch surgical technique for 41. Doumouchtsis SK, Nikolopoulos K,
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and long-term results (author’s transl). rhage: an alternative to hysterectomy? Five strual and fertility outcomes following the

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surgical management of postpartum haemor- hemorrhage. Int J Gynaecol Obstet 2010;108: morbidity [second annual report]. Aberdeen:
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B-Lynch suture hidden long-term effects? Fertil ternal iliac artery ligation in obstetric hemorrhage 48. Doumouchtsis SK, Papageorghiou AT,
Steril 2010;94:e62. with the current gain in popularity of other uterus Arulkumaran S. The surgical management of
43. Sentilhes L, Gromez A, Trichot C, Ricbourg- sparing techniques? J Matern Fetal Neonatal intractable postpartum hemorrhage. Acta
Schneider A, Descamps P, Marpeau L. Fertility Med 2017;30:1325–32. Obstet Gynecol Scand 2009;88:489–90.
after B-Lynch suture and stepwise uterine 46. Shellhaas CS, Gilbert S, Landon MB, et al. 49. Amorim-Costa C, Mota R, Rebelo C,
devascularization. Fertil Steril 2009;91:934.e5–9. The frequency and complication rates of hys- Silva PT. Uterine compression sutures
44. Sentilhes L, Gromez A, Marpeau L. Fertility terectomy accompanying cesarean delivery. for postpartum hemorrhage: is routine
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and B-Lynch suture to control postpartum Scottish confidential audit of severe maternal 701–6.

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SUPPLEMENTAL FIGURE 1
Hayman’s uterine compression technique32

A, Two double independent mediolateral vertical braces on the right and left, which can be placed
after the hysterotomy incision has been closed.

- The needle (for example, a straight needle with No. 0 polyglactin 910 suture) crosses the anterior
and posterior walls of the uterus approximately 2 to 3 cm under the sutured hysterotomy incision,
at 3 to 4 cm from the left lateral edge.
- This first suture is “doubled,” that is, an adjacent second suture now also crosses the anterior and
posterior walls of the uterus, approximately 2 to 3 cm under the sutured hysterotomy incision, 3 to
4 cm from the left lateral edge.
- With a third suture, the needle crosses the anterior and posterior walls of the uterus approximately
2 to 3 cm under the sutured hysterotomy incision, at 3 to 4 cm from the right lateral edge.
- This third suture is also doubled; that is, an adjacent fourth suture now also crosses the anterior
and posterior walls of the uterus approximately 2 to 3 cm under the sutured hysterotomy incision,
3 to 4 cm from the right lateral edge.
- Both ends of the first suture are then pulled, aided by the assistant’s manual compression, so that
the anterior and posterior walls touch each other. Both sutures are then tied together at the level of
the uterine fundus.
- The same procedure is repeated for the 2 strands of the second, third, and fourth sutures.

B, Lateral view, visualization of 1 of the 4 sutures.


Bouchghoul. Uterine-sparing surgical procedures. Am J Obstet Gynecol 2022.

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SUPPLEMENTAL FIGURE 2
Pereira’s uterine compression technique33

A, Anterior view. The superior transverse suture passes through the right and left broad ligaments of
the uterus high in the avascular area (just under the 2 uterine horns) and is tied at the anterior wall of
the uterus: (1) beginning of the superior transverse suture; (2) the superior transverse suture passes
through the left broad ligament of the uterus, high up in the avascular area; (3) end of the superior
transverse suture; and (4) the superior transverse suture is tied at the anterior wall of the uterus. B,
Posterior view. The 3 transverse sutures are in place and tied at the anterior wall of the uterus (1, 2,
3). On the posterior wall, a longitudinal suture (4) is tied to the transverse suture (5) situated at the
level of the lower segment. The suture is directed toward the uterine fundus; at the superior posterior
wall, it superficially transfixes the myometrium, with the aid of the needle, before reaching the uterine
fundus. Once at the fundus, the suture runs anteriorly along the anterior surface, which it also
transfixes superficially through the myometrium in its superior portion, then descends and is finally
tied on the anterior wall to the transverse suture located at the level of the lower uterine segment.
Bouchghoul. Uterine-sparing surgical procedures. Am J Obstet Gynecol 2022.

10.e2 American Journal of Obstetrics & Gynecology MONTH 2022


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SUPPLEMENTAL FIGURE 3 SUPPLEMENTAL FIGURE 4


Uterine compression by a Bhal’s uterine compression technique34
variation of the Hayman
technique

Two mediolateral independent vertical braces on


the right and left, not 2 on each side. They can A, This has the advantage of uterine compression based on B-Lynch’s principles (braces) and can be
be placed after the hysterotomy incision has performed with the incision closed. B, For each brace, the needle goes through only twice: the first
been closed. There are then only 2 transfixing passage of the needle (1) goes through the anterior and posterior uterine walls, 3 cm beneath the
sutures. (closed) incision. The suture thus moves along the posterolateral wall of the uterus, toward the
Bouchghoul. Uterine-sparing surgical procedures. Am J uterine fundus, and then goes back down along the anterolateral wall of the uterus. The needle then
Obstet Gynecol 2022.
transfixes the anterior wall of the uterus, 3 cm above the (closed) incision to reemerge 2 cm below
the incision (exit point 3), or 1 cm above the first input point (A). The same procedure is performed for
the second, that is, left brace. C, The strands of the primary exit points (3 and 6) of the 2 braces are
then tied together (forming a first transverse suture at the lower segment, 3 cm under the incision);
the strands of the primary entrance points (1 and 4) of the 2 braces are then tied together (forming a
second transverse suture at the level of the lower segment, 4 cm under the incision).
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SUPPLEMENTAL FIGURE 5
Ouahba’s uterine compression
sutures30

Technique based on 4 sutures: a suture in the


right uterine horn (1), mirrored by another suture
in the left uterine horn (2), a transverse suture in
the middle of the uterine body, and another
transverse suture at the level of the lower uterine
segment, below the sutured incision.
Bouchghoul. Uterine-sparing surgical procedures. Am J
Obstet Gynecol 2022.

10.e4 American Journal of Obstetrics & Gynecology MONTH 2022

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