Arch Gynecol Obstet

DOI 10.1007/s00404-016-4009-x

MATERNAL-FETAL MEDICINE

Uterine folding hemostasis: a simpler and safer technique

for controlling atonic postpartum hemorrhage
Guang-Tai Li1,3 • Guang-Rui Li2 • Hong-Mei Xu3 • Bao-Ping Wu1,3 •

Xiao-Nian Wang4

Received: 13 June 2015 / Accepted: 5 January 2016

Ó Springer-Verlag Berlin Heidelberg 2016

Abstract bleeding after the procedure. There were no morbidities or

Objective To observe the efficacy and safety of a uterine abnormalities of the uterus in these 32 patients. Eight
folding hemostatic technique in controlling atonic post- women had pregnancies after this hemostasis and the oth-
partum hemorrhage (PPH) during cesarean delivery. ers lacked the desire for future pregnancy.
Methods Thirty-nine women with severe postpartum Conclusion Uterine folding hemostasis is a simple, safe
bleeding from uterine inertia, which did not react to con- and effective technique to control the atonic PPH.
ventional initial management protocols, underwent a uter-
ine folding hemostasis. The procedure was to fold the Keywords Uterine folding hemostasis
Postpartum
uterine fundus onto the anterior wall of the corpus uterus hemorrhage
Uterine atony
Uterine compression suture
using an absorbable suture that thread tautly through the
inner myometrial layer of the uterus 1–3 cm below the
fundus (not entered into uterine cavity) and 1–2 cm above Introduction
and below the CS incision (entered into uterine cavity
2–4 cm medal to bilateral border of the uterus). Atonic postpartum hemorrhage (PPH) is a potentially
Results The technique was sufficient to stanch bleeding serious complication of labor and delivery in which the
immediately in 32 patients (82.1 %). Seven women uterus fails to clamp down after delivery, and blood flows
underwent hypogastric arteries ligation (1 case) or uterine freely. PPH remains a major cause for maternal mortality
arterial embolization (6 cases) because of continuous throughout the world, accounting for 30 % or more of all
maternal deaths [1–4]. However, 90 % of maternal deaths
due to PPH could be avoided by prevention strategies,
G.-T. Li and G.-R. Li contributed equally to this study and share first appropriate diagnosis and management [4, 5]. It is there-
authorship. fore recommended that active management of the third
& Guang-Tai Li
stage of labor (AMTSL) be offered to all women during
lgt93@126.com childbirth by a skilled attendant to prevent PPH [6].
Techniques to address it immediately involve blood vol-
1
Department of Obstetrics and Gynecology, China Meitan ume restoration and bleeding control. The latter includes
General Hospital, No.29 Xibahe Nanli, Chaoyang District,
100028 Beijing, People’s Republic of China
medications to facilitate uterine cramping, manual com-
2
pression of the uterus to stop the bleeding and surgical
China Academy of Chinese Medical Sciences, Wangjing
Hospital, Huajiadi Jie, Chaoyang District, 100102 Beijing,
options. In the surgical therapeutics, a good result has
People’s Republic of China been obtained by uterine compression sutures (UCS) [1,
3 6–8], but various complications related to UCS have also
Department of Obstetrics and Gynecology, Beijing Fengtai
Hospital, No. 1 Xi’an Jie, Fengtai District, 100071 Beijing, been continuously reported in the literature [7, 8].
People’s Republic of China Therefore, how to reduce the side effects and complica-
4
Fengtai Maternal and Child Hospital, Caihuying, Fengtai tions of UCS has become one of the highlights on this
District, 100069 Beijing, People’s Republic of China technique.

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 Arch Gynecol Obstet

In this paper, we report on a novel uterine compression pulled tautly and finally tied together with a fourfold flat
hemostatic method based on our previous research [9], knot as tightly as possible (Fig. 1, Fig. 2).
uterine folding hemostasis (Li’s folding hemostatic tech- Concurrent therapy including blood transfusion, plasma
nique), which can achieve the same effect as other UCS expanders, anti-shock measures and fibrinogen was also
and can have lesser complications. administered depending on the patient’s needs. Postoper-
ative patient management and length of hospital stay were
similar to those in patients who underwent ordinary
Materials and methods cesarean section (CS). Antibiotics were administered to all
women who underwent a CS and were continued postop-
The study was conducted from December 2006 to eratively for at least 5 days.
November 2014, at the China Meitan General Hospital and For all patients, the follow-up was conducted 6 weeks
Beijing Fengtai Hospital. Data on the patient’s age, number after hospital discharge. Additional follow-ups were car-
of gravidities, parity, gestational age at birth, diagnosis at ried out every 3 months for the first year and then annually.
presentation, mode of delivery, neonatal weight, amount of The patients’ medical records were reviewed to evaluate
blood loss, volume replacement, recovery of normal men- the effectiveness of the hemostatic technique. The patients
strual flow and complications were collected. Their char- were informed about the PPH and advised to have close
acteristics are listed in Table 1. gynecological follow-up examinations, including ultra-
The uterine folding hemostasis was performed for PPH sonography and a control hysteroscopy, after 6 months.
caused by uterine atony in 39 women whose blood loss was
failed to stop after initial routine management (i.e.,
bimanual uterine massage, gauze packing, appropriate Results
uterotonic agents, etc.). Cesarean deliveries were per-
formed by third-year obstetric residents under the guidance The age of the 39 patients with atonic PPH was between 22
of staff obstetricians. The operations of uterine folding and 41 years (28.64 ± 5.11 years, mean ± SD). Parity
hemostasis were performed by staff obstetricians who were ranged from 0 to 1, the gestational age at which the pro-
trained to perform the technique under the guidance of cedure was performed ranged from 36 weeks plus 6 day to
senior surgeon. The application of this technique was 41 weeks plus 3 days (mean 37 weeks plus 3 days).
approved by both hospitals’ Ethics Committee and a Neonatal weight was between 3530 and 4490 g
written informed consent form had been signed by the (3968.97 ± 469.31 g). All patients manifested uterine
women and/or their nearest relatives before the operation. hypotony. The majority of the patients (30/39) were
In all subjects, the uterus was opened using a low primipara. All 39 cases had undergone conservative man-
transverse incision. After the placenta was removed, the agement (i.e., uterotonic drugs such as oxytocin and/or
bladder was separated from the lower uterine segment and prostaglandin analogs, manual massage and gauze packing)
reflected downward behind a retractor to expose the uterine but did not respond. The technique was sufficient to stanch
lower segment. A 70 mm round needle (or a 65 mm liver bleeding immediately in 32 patients. The rate of effec-
needle) with Vicryl No. 1 absorbable thread (Ethicon, Inc., tiveness was 82.1 % (32/39). Seven women underwent
Somerville, NJ, USA) was entered into the uterus 1–2 cm hypogastric arteries ligation (1 case) or uterine arterial
below the left lower edge of the uterine incision and embolization (6 cases) after the procedure for continu-
2–3 cm medial to the left lateral border of the lower uterine ous small flow bleeding coming from the uterus.
segment, guiding the thread into the uterine cavity to Total operation time was between 60 and 130 min
emerge 1–2 cm above the upper incision margin and (73.03 ± 12.39 min). The time consuming of this proce-
approximately 3–4 cm from the left lateral border of the dure was from 5 to 11 min (8.05 ± 1.41 min).
uterus. It was then carried upward along the anterior aspect The total blood loss ranged from 1200 to 3100 ml
of the uterus to pierce the uterus 1–3 cm below the fundus (2097.44 ± 469.31). Thirty-seven women received blood
and about 4 cm medial to the left cornu, and threaded transfusions (1–8 packed red blood cell units;
through the inner myometrial layer (not entered into uterine 724.32 ± 337.81 ml) and fresh-frozen plasma transfusions
cavity) emerging from the serosa of the posterior wall. The and all patients achieved a good postoperative recovery.
suture material was carried horizontally to the right punc- Five of the women were kept in the intensive care unit for
ture point, which was symmetry for the left, pressing the 24 h. Delayed hemorrhage was found in six patients and
needle from back to outside of anterior wall. Then, the remedied for uterine arterial embolization. Other patients
suture was downwards to place as the left suturing line but were not found continuously bleeding up to the time when
in the opposite direction. The two ends of the thread were they were discharged from the hospital on day 7 after the

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 Table 1 Characteristics of patients with atonic PPH treated by uterine folding hemostasis
Case Age Gravidity Term (weeks Mode of Neonatal Estimated Blood transfusion Operative time/ Adjunctive Resumed Follow-up
No. (years) and parity of gestation) delivery weight (g) blood loss (unit) hemostatic time hemostatic menstruation/got (months)
(ml) (min) procedures gestation (months)

1 25 G2P0 39 ? 2 CS 3930 1600 2 units PRBC 65/9 3 95

Arch Gynecol Obstet

2 27 G1P0 38 ? 4 CS 4230 2000 3 units PRBC 73/7 4 48

200 ml FFP
3 25 G2P0 40 ? 1 CS 3780 1800 3 units PRBC 80/8 3/39 63
200 ml FFP
4 35 G3P1 39 ? 5 CS 4310 2600 5 units PRBC 80/10 UAE 5 52
600 ml FFP
5 27 G3P0 36 ? 6 CS 3850 1200 0 units PRBC 60/6 3 75
6 22 G3P1 37 ? 2 CS 3980 1500 1 units PRBC 70/8 3/35 91
7 41 G2P0 38 ? 6 CS 4120 2800 5 units PRBC 75/9 UAE 4 55
400 ml FFP
8 26 G2P0 39 ? 3 CS 3880 2000 3 units PRBC 65/7 3 48
200 ml FFP
9 23 G2P0 38 ? 5 CS 3920 2200 4 units PRBC 70/6 4/25 47
400 ml FFP
10 24 G1P0 37 ? 1 CS 3910 2400 5 units PRBC 70/5 UAE 4 70
600 ml FFP
11 28 G2P0 38 ? 6 CS 4490 3100 8 units PRBC 130/6 HAL 4 85
600 ml FFP
12 29 G3P0 39 ? 2 CS 3530 1400 0 units PRBC 75/9 2 29
13 26 G3P1 40 ? 3 CS 3840 1800 3 units PRBC 80/10 3 43
14 32 G3P0 39 ? 2 CS 3950 2600 5 units PRBC 90/8 4 54
200 ml FFP
15 26 G3P0 38 ? 4 CS 3890 2300 4 units PRBC 85/8 3/30 67
400 ml FFP
16 31 G1P0 38 ? 5 CS 3600 1700 2 units PRBC 60/7 3 42
17 40 G3P1 37 ? 4 CS 4040 2600 5 units PRBC 85/11 4 28
400 ml FFP
18 24 G1P0 38 CS 3900 1800 2 units PRBC 65/7 3 39
19 23 G2P0 37 ? 6 CS 3750 2100 4 units PRBC 65/8 3 77
200 ml FFP
20 35 G1P0 38 ? 5 CS 4120 2500 5 units PRBC 68/9 4 72
400 ml FFP
21 22 G1P0 37 ? 3 CS 3750 1900 3 units PRBC 60/8 3/26 63

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 Table 1 continued
Case Age Gravidity Term (weeks Mode of Neonatal Estimated Blood transfusion Operative time/ Adjunctive Resumed Follow-up
No. (years) and parity of gestation) delivery weight (g) blood loss (unit) hemostatic time hemostatic menstruation/got (months)

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(ml) (min) procedures gestation (months)

22 37 G2P1 38 ? 1 CS 3990 2800 6 units PRBC 75/9 4 58

600 ml FFP
23 30 G3P0 40 ? 2 CS 3950 3000 7 units PRBC 90/11 UAE 4 52
600 ml FFP
24 25 G1P0 40 ? 4 CS 4300 2200 4 units PRBC 72/9 3 37
200 ml FFP
25 34 G2P0 39 ? 2 CS 4150 1600 2 units PRBC 65/6 3 46
26 23 G1P0 39 ? 5 CS 3720 2200 4 units PRBC 80/8 3/46 87
200 ml FFP
27 27 G3P0 41 ? 1 CS 3880 1800 2 units PRBC 70/9 3/37 81
200 ml FFP
28 29 G2P1 39 ? 5 CS 4250 2700 6 units PRBC 75/10 UAE 4 66
400 ml FFP
29 32 G4P1 40 ? 1 CS 3990 2800 6 units PRBC 80/9 UAE 4 25
400 ml FFP
30 26 G2P0 39 ? 6 CS 3960 2000 3 units PRBC 75/8 3/28 49
200 ml FFP
31 28 G2P0 40 ? 1 CS 3890 1500 2 units PRBC 60/6 3 30
32 25 G1P0 38 ? 6 CS 3870 1800 2 units PRBC 60/7 3 29
33 23 G2P0 41 ? 3 CS 4020 2000 2 units PRBC 70/9 3 40
200 ml FFP
34 33 G1P0 39 ? 5 CS 3900 1600 1 units PRBC 65/8 4 16
200 ml FFP
35 28 G3P1 38 ? 4 CS 4130 1800 2 units PRBC 65/8 3 11
36 37 G1P0 38 ? 3 CS 3980 2100 4 units PRBC 70/9 4 7
200 ml FFP
37 26 G2P0 39 ? 4 CS 4210 2200 4 units PRBC 65/7 3 12
400 ml FFP
38 27 G4P1 38 ? 5 CS 3880 2000 3 units PRBC 70/7 3 23
200 ml FFP
39 36 G1P0 39 ? 6 CS 3950 1800 2 units PRBC 70/8 3 18
200 ml FFP
CS cesarean sections; PRBC packed red blood cells; FFP fresh-frozen plasma; UAE uterine arterial embolization; HAL hypogastric arteries ligation
Arch Gynecol Obstet
Arch Gynecol Obstet

operation. The time of follow-up in all women was conservation of the uterus for subsequent menstrual func-
49.56 ± 23.58 months (ranged 7–95 months). tion and pregnancies, the complications related to these
In all patients who had undertaken the procedure, no techniques, such as pyometra, ischemic uterine necrosis,
morbidities or abnormalities of the uterus or pelvic cavity uterine suture erosion and uterine synechiae acute or
related to this technique were found by gynecological chronic inflammation, etc., have been postoperatively
examination, abdominal ultrasound and hysteroscopic reported by some authors [7, 8, 15, 17, 18]. Furthermore,
evaluation after 6 months following the procedure. Post- UCS may cause fertility problems, even though the pro-
partum menstrual flow and breastfeeding were normal. The cedure is intended to preserve fertility.
time periods for the patients’ menstruation to resume were As other UCS hemostatic techniques, the uterine folding
between 2 and 5 months (3.38 ± 0.59 months). No post- hemostasis enables us to avoid emergency hysterectomy in
operative symptoms, including lower abdominal com- the vast majority of patients and thus preserves their fer-
plaints, were reported. tility and obviates any other surgical complications of
Eight women had pregnancies after this hemostasis. The hysterectomy under the critical circumstance. The success
other patients did not desire to become pregnant because rate of the procedure is 82.1 % (32/39) in our series of 39
they were possibly afraid of recurring PPH. These subse- patients, which is comparable to previous reports on vari-
quent pregnancies occurred between 25 and 46 ous hemostatic methods for atonic PPH [7, 8, 10–12, 15].
(33.25 ± 7.29) months after the procedure and delivered Even though seven women received the treatment of
by repeat CS. No abnormalities of the uterus and pelvic hypogastric arteries ligation and uterine arterial emboliza-
cavity related to previous uterine folding hemostasis were tion after the procedure, they presented a small flow
found during these repeat CSs. bleeding coming continuously from the uterus which was
lesser than before the operation. Besides, all these cases
made a good postoperative recovery. The follow-up
Discussion revealed that none of them developed complications related
to the procedure as other UCS techniques, such as necrosis,
PPH is a life-threatening condition and should be managed infection, synechia, adhesions, uterine wall dehiscence,
without wasting time. Most cases of PPH are due to uterine irregular menstruation or menstruation-associated pain
atony. Methods to treat it can include medications to symptoms [7, 8, 15, 19]. The evaluation of the uterus (e.g.,
facilitate uterine cramping, manual compression of the gynecological examination, ultrasound and diagnostic
uterus to stop the bleeding and surgical options. It usually hysteroscopy after the procedure) showed normal uterine
responds to uterotonic drugs (e.g., oxytocin, ergometrine cavities. The inspections of re-laparotomy for repeat CS in
and prostaglandins [1, 5–8]), bimanual uterine massage and eight women with subsequent pregnancies were also not
hot compress (pressing with warm gauzes). Should these found, any abnormalities in the uterus and pelvic cavity.
measures fail, various organ preserving simple procedures The mechanism of uterine folding hemostasis for
(e.g., uterine balloon tamponade or gauze packing) can be reducing or stopping bleeding is to enhance the pressure on
attempted before other complex treatment alternatives are the endometria by apposing both walls of the uterus toge-
considered. Uterine-sparing surgical methods to reduce ther when overlapping the fundus on the anterior wall of
arterial pulse pressure in the pelvis have been described,
from ligation of the uterine arteries to that—more com-
plicated—of the internal iliac arteries, and to embolization
of uterine arteries or temporary intra-aortic balloon
occlusion of the lower abdominal aorta. In extreme cases, it
might be necessary to remove the uterus to stop the
bleeding. However, this can be very traumatic for the
patient who will have to bear the risk of possible surgical
complications and subsequent infertility forever [10–15].
New techniques to address hemorrhage while retaining
fertility are a constant topic of research, in which UCS is
the best form of surgical approach for controlling atonic
PPH as it helps in preserving the anatomical integrity of the
uterus [16]. Since B-Lynch reported a brace UCS in 1997,
various UCSs have been devised to control postpartum
Fig. 1 Sagittal section of the uterine folding hemostasis. The arrows
hemorrhage (PPH) [7, 8, 15]. Although these sutures have indicate the direction and line of the suture; the numbers represent the
achieved good therapeutic effectiveness and allowed for puncture point and the pierce sequence

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 Arch Gynecol Obstet

the uterus. Our experience showed that, for atonic PPH, as

long as both walls of the uterus were closely approximated
together, the pressure occurring between them will be
enough to resist the potence of bleeding on the endometria,
which is also the rationale of UCS to control PPH [7, 9, 15,
18, 20–22].
In addition to enabling these patients to avoid emer-
gency hysterectomy and complications related to hys-
terectomy, the uterine folding hemostasis has a lot of
advantages as follows: (1) It only uses one thread, which is
relatively more cost-effective. (2) The procedure is simple,
fast and easy to perform, thus it requires less skill when
compared with other UCS, because its suture is directly
into the fundus’s wall but not into the outer of the uterus,
which can avoid high operative risks, and make us not fear
that there are important structures such as greater vessels or
ureter in its surroundings. (3) The residual part of the
suturing thread is very short and the most of it is also Fig. 3 Anterior view of the uterine folding hemostasis with closed
buried under the bladder peritoneum, which prevents it CS incision or without hysterotomy. The arrows indicate the direction
from forming a loop after uterine retraction and resulting in and line of the suture; the numbers represent the puncture point and
the pierce sequence
the intussusception of the guts. (4) It not only keeps the
anteversion position of the uterus but also avert uterine
inversion. (5) It is not easy to raise the infection, adhesion place the suture in the lower segment uterine wall (Fig. 3),
or occlusion of the uterine cavity and endometriosis, which reduces the time of surgical suture, provides an
because the stitch does not transfix through the uterine opportunity to lessen blood loss and also decreases the
cavity. (6) It will be not apt to cause uterine ischaemic therapeutical charges.
necrosis and hence practitioner does not worry about the In summary, though the evidence for the use of this
thread being pulled too tight, because the thread exerts a folding hemostasis is based on case series without proper
compression effect on the myometrium by folding the control groups, it is apparent that the procedure is suc-
uterus in marked anteflexion to apposed both walls of the cessful in most patients and should be incorporated or even
uterus together rather than directly squeezing the uterine be the first-line surgical management for PPH due to
wall. (7) If atonic PPH occurs in vaginal delivery or after uterine inertia. The drawbacks in our data are the limited
the uterine incision has been closed during CS, it is not number of patients and the success rate that seems a little
required to open or re-open the incision and may directly lower than that of other documents [7, 8, 15]. It is still
required for a long-term observation to determine its effi-
cacy and safety. We are currently enrolling more patients
to further compare our technique with other uterine
hemostasis and to obtain more evidence for the effective-
ness and the safety of this technique.

Authors’ contributions GT Li conceived the idea, designed and

performed the surgical procedure, drafted the manuscript and figures.
GR Li conceived the initial idea, developed the project and supervised
the experiments. HM Xu, BP Wu and XN Wang collected and ana-
lyzed the data, wrote the manuscript, observed the complications and
developed the illustrations and figures.

Funding source No funding source was involved.

Compliances with ethical standards The study protocol had been

approved by The Local Ethical Committee of Meitan General
Hospital.
Fig. 2 Anterior view of the uterine folding hemostasis with unclosed
CS incision. The arrows indicate the direction and line of the suture; Conflict of interests The authors declare that they have no conflict
the numbers represent the puncture point and the pierce sequence of interest.

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Arch Gynecol Obstet

Disclosure statement The authors declare that we have no financial caesarean section for placenta praevia accreta. Arch Gynecol
and personal relationships with other people or organizations that can Obstet 278(6):555–557
inappropriately influence their work; there is no professional or other 11. Ajenifuja KO, Adepiti CA, Ogunniyi SO (2010) Postpartum
personal interest of any nature or kind in any product, service and/or haemorrhage in a teaching hospital in Nigeria: a 5-year experi-
company that could be construed as influencing the position presented ence. Afr Health Sci 10(1):71–74
in, or the review of, the manuscript entitled. 12. Shabana A, Fawzy M, Refaie W (2015) Conservative manage-
ment of placenta percreta: a stepwise approach. Arch Gynecol
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