International Journal of Gynecology and Obstetrics 128 (2015) 122125

Contents lists available at ScienceDirect

International Journal of Gynecology and Obstetrics

journal homepage: www.elsevier.com/locate/ijgo

CLINICAL ARTICLE

Cervical inversion as a novel technique for postpartum hemorrhage

management during cesarean delivery for placenta
previa accreta/increta
Nahid Sakhavar a, Zahra Heidari b,, Hamidreza Mahmoudzadeh-Sagheb b
a
Pregnancy Health Research Center and Department of Gynecology and Obstetrics, School of Medicine, Zahedan University of Medical Sciences and Health Services, Zahedan, Iran
b
Genetics of Non-communicable Disease Research Center and Department of Histology, School of Medicine, Zahedan University of Medical Sciences and Health Services, Zahedan, Iran

a r t i c l e i n f o a b s t r a c t

Article history: Objective: To describe the use of cervical inversion for postpartum hemorrhage (PPH) management during
Received 15 March 2014 cesarean delivery for placenta previa accreta/increta. Methods: In a retrospective, descriptive study, data were
Received in revised form 20 August 2014 reviewed for cases in which cervical inversion was used to manage PPH during cesarean delivery at a center in
Accepted 20 October 2014 Zahedan, Iran, between July 2, 2011, and September 25, 2014. Cervical inversion was applied when placental
bleeding was persistent and the sites could not be clearly located. The cervix is inverted using ring forceps or
Keywords:
straight Allis forceps, after which the placental bed is sutured to control bleeding. After bleeding is controlled,
Cervical inversion
Cesarean delivery
the cervix is returned to its original position. Results: Cervical inversion was successfully applied to 10 cases.
Placenta accreta Mean time to completion of cervical inversion was 4.1 0.7 minutes. In all 10 cases, the bleeding was stopped
Placenta increta within 35 minutes from the beginning of the cervical inversion procedure. No apparent complications were
Placenta previa reported, and blood transfusions or obstetric hysterectomies were not necessary. Conclusion: Cervical inversion
Postpartum hemorrhage is a simple, cost-effective, and time-saving procedure for PPH management in placenta previa accreta/increta.
It could become a routine procedure for preserving the uterus and fertility of affected women.
2014 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.

1. Introduction and diabetes, pregnancy after in vitro fertilization, hydramnios, and

Maternal mortality is approximately 14% in low-income countries,
and 4% in high-income countries [1]. Postpartum hemorrhage (PPH)
remains a major leading cause of direct maternal mortality [2,3],
accounting for almost half of all postpartum deaths in low-resource
countries [4].The denitive treatment for severe PPH is hysterectomy,
but this procedure is associated with intraoperative comorbidity and
postpartum depression, and compromises fertility [5]. As a result,
other surgical procedures should be considered initially [6].
Bleeding from the placental bed should be controlled by strong
myometrial contractions and constriction of blood vessels. The absence
of these mechanisms in placenta previapartial or complete coverage
of the internal cervical orice by placental tissue [7]can lead to PPH
[5]. The risk factors for placenta previa include implantation in the
lower segment over a surgical scar, advanced maternal age, smoking,
multiparity, previous placenta previa, alcohol and illicit drug use, spon-
taneous and induced abortions, multiple pregnancy, maternal anemia
Corresponding author at: Department of Histology, School of Medicine, Zahedan
University of Medical Sciences, Zahedan, 98167-43463, Iran. Tel./fax: +98 541 3414572.
E-mail address: histology@ymail.com (Z. Heidari).
chronic hypertension [79].
The severe bleeding observed among women with placenta previa
arises because the lower uterine segment is morphologically and func-
tionally different from the upper segment [7]. The highly vascular
lower segment is slow to retract, which causes severe blood loss [7,
10]. When uterotonic drugs fail, surgical interventions or other proce-
dures are needed to control bleeding. Over-sewing of the bleeding
sites, uterine compression sutures, ligation or embolization of uterine
and hypogastric arteries, and intrauterine balloon tamponade are the
most common procedures used to control bleeding [11]. Over-sewing
of the bleeding site is the most common procedure used for PPH man-
agement, but in many cases, the bleeding points located in the lower
segment and cervical canal are too deep and their locations are unclear
because of the severity of the bleeding [3].
The aim of the present study was to describe and present data from a
novel techniquecervical inversionfor PPH management in cases of
placenta previa accreta/increta. In this maneuver, the cervix and lower
segment are inverted through the Kerr incision into the uterus by
using ring or straight Allis forceps. The procedure transiently blocks
blood vessels and reduces the bleeding, thereby providing direct visual-
ization and better access to the bleeding sites during the suturing
procedure.

http://dx.doi.org/10.1016/j.ijgo.2014.08.020
0020-7292/ 2014 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
 N. Sakhavar et al. / International Journal of Gynecology and Obstetrics 128 (2015) 122125 123

2. Materials and methods 3. Results

In a retrospective, descriptive study, data were reviewed for cases in
which cervical inversion was used at the Zahedan University of Medical
Sciences and Health Services, Zahedan, Iran, between July 2, 2011, and
September 25, 2014. This technique had been used in women with
placenta previa and placenta accreta/increta who experienced PPH
during cesarean delivery. The ethics committee of Zahedan University
of Medical Sciences approved this study. All patients provided written
informed consent.
Women with placenta previa are always managed by cesarean
delivery at the study hospital. After delivery of the fetus and the placen-
ta, an inspection and palpation of the uterine cavity is performed to
gently exclude as much retained placental tissue as possible. At the
same time, the uterus is massaged and suitable oxytocic and uterotonic
drugs are administered. Since 2011, the cervical inversion technique has
been used for all women with placenta previa and placenta accreta/
increta whose bleeding persists after these steps.
For cervical inversion, the surgeon enters his/her index nger into
the lower segment and cervical canal until it touches the cervical lips.
Then, he/she grasps the anterior or posterior cervical lip using a suitable
instrument such as ring forceps or straight Allis forceps. The cervix is
inverted into the uterus by pulling the instrument back through the
Kerr incision (Figs. 1 and 2). After this maneuver, the placental bed is
sutured to control the bleeding. The cervix is then pushed back to its
original position and the Kerr incision is repaired.
During the study period, cervical inversion was applied by N.S. to 10
cases of placenta previa with concurrent placenta accreta/increta. The
mean age of the patients was 26.3 4.5 years. Eight women had had
either two or three previous deliveries by cesarean, one was primipa-
rous, and the other had had one previous vaginal delivery.
The mean time to complete cervical inversion was 4.1 0.7 mi-
nutes. In all 10 cases, the bleeding was stopped within 35 minutes
from the beginning of the cervical inversion procedure. No difculties
were recorded in performing the procedure, and there was no trauma
to the lower segment of the uterus or cervix in any of the women.
Furthermore, there was no need for blood transfusion owing to blood
loss during the cesarean delivery and no requirement for obstetric
hysterectomy.
4. Discussion
Cervical inversion was used for the rst time in 2011 in an attempt to
manage PPH in a young woman with placenta previa and focal placenta
increta, while preserving her uterus and future fertility. As reported in
the present study, this procedure has since been effectively applied to
nine further cases with no apparent complications. On the basis of the
present results, cervical inversion could be a reasonable method for
successful management of PPH in cases of placenta previa diagnosed
by clinical evidence. The technique is effective and simple: the surgeon

Fig. 1. Schematic illustrations of cervical inversion. (A) Horizontal incision of the uterus (Kerr incision). (B) Inversion of the cervix and lower segment into the uterus; the inverted region is
shown as a dotted line. (C) Inversion of the cervix and lower segment into the uterus; a window has been removed for better observation of the inverted region. (D) Repair of the Kerr
incision after the cervix has been returned to its Original position. Figure published with the permission of the artist, Zahra Heidari.
124 N. Sakhavar et al. / International Journal of Gynecology and Obstetrics 128 (2015) 122125
Fig. 2. Image of the inverted cervix in a case of placenta previa.
can see the bleeding sites directly and thus avoid further tears,
narrowing of the cervical canal, and needle site bleeding.
There are various methods to prevent and manage PPH. Use of
uterotonics is the rst step in controlling bleeding; if the drugs fail,
other techniques such as uterine tamponade and gauze packing, a
Foleys catheter, SengstakenBlakemore tube, or Bakri balloon can be
applied [12]. Treatment of severe PPH by uterine or hypogastric artery
ligation and arterial embolization is effective, but these approaches
can be difcult to perform in practice and complications have been
reported [10]. As described in previous studies [13,14], the reasons for
low use of uterine artery embolization include the small number of
modern angiography units with an experienced skilled team on-call
24 hours per day and the perceived risk of transferring a patient in
unstable condition to the angiography suite.
Johanson et al. [15] described a method of tamponade using a hydro-
static balloon catheter. However, the major disadvantage of packing the
uterus is that the bleeding can continue but remain obscure for a while.
In cases of profuse bleeding, precise identication of the bleeding site
might be difcult. Applying blind compression suturese.g. transverse
annular, parallel vertical, or circular isthmic-cervical suturescan be
associated with further complications, including uterine cavity closure,
infection, and pyometra due to blood entrapment, intrauterine adhe-
sions, and partial uterine wall necrosis. Furthermore, repeated blind
sutures will result in further loss of critical time. By contrast, surgeons
can see the bleeding sites directly and control them with fewer sutures
using cervical inversion.
Another conservative surgical technique is the B-Lynch or brace
suturing technique, in which pressure is applied by the compression
sutures. This method can cause progressive total or partial myometrial
ischemic necrosis and myometrial defects, which might be hazardous
in future pregnancy. In addition, it is only applicable to bleeding in the
upper segment [3]. Moreover, surgeons experienced in this procedure
might not be readily available everywhere.
Matsubara et al. [16] introduced cervix-holding by round forceps
placed simultaneously over the anterior and posterior cervical lips to
control hemorrhage after cesarean delivery for placenta previa. They
stated that hemostasis was achieved by this method for two main
reasons. First, the intrauterine blood is able to compress the bleeding
surface, and second, handling the cervix might create uterine contrac-
tions and control bleeding. It seems likely that cervical inversion
might have a similar effect on uterine contractions.
The cervical inversion procedure transiently decreases the vascular
blood ow to the lower uterine segment, leading to rapid hemostasis.
The uterine lower segment is supplied by three principal arterial
branches: an upper branch formed by the uterine artery, a middle
branch constituted by the cervical artery, and a lower one made up by
the vaginal arteries. These arteries anastomose with each other along
the border between the uterine isthmus and vagina, or in the intramural
part of the cervico-vaginal junction. In certain pathologic conditions
such as placenta percreta, unusual interconnections form among these
arteries, which can lead to difculties and failure to control bleeding
and hemostasis [17]. In these situations, uterine anastomotic interac-
tions may cause alterations in the arterial ow between the uterine
and vaginal arteries [18]. When the cervix is inverted, the pressure on
vessels in the lower segment transiently blocks them and reduces
blood ow, providing additional time for suturing the bleeding points
on the placental bed.
After cesarean delivery, poor healing of the uterine scars might affect
regeneration of the uterine isthmus, making the lower segment thin
and weak during subsequent pregnancies. The American College of
Obstetricians and Gynecologists recently suggested that the absolute
risk of uterine dehiscence in repeated cesarean is low, and that most
women with one prior low-transverse cesarean should be offered the
opportunity of labor [19].The cervical inversion technique might be
applicable to repeated cesarean procedures for several reasons. First,
the Kerr incision is made in the middle of the previous scar and thus
might reduce its diameter. Second, if the procedure is performed imme-
diately after delivery of the neonate and placenta, the lower segment
will be relatively soft and easily inverted. Third, almost all women
with placenta previa have a planned cesarean delivery or are referred
for emergency cesarean immediately after the beginning of parturition
bleeding before advanced dilatation or effacement (ripening) of the
cervix and severe bleeding occurs; as a result, in almost all cases, the
cervix is unripe and the lower segment is in a tensile state, such that
grasping the cervical lip and inverting the cervix will be simple.
The cervix softens during pregnancy, which is essential for cervical
effacement and dilatation and successful labor and childbirth. It is
thought that prostaglandins, together with relaxin, can induce cervical
softening by inducing collagen breakdown within the tissues and/or
by altering the glycosaminoglycan (GAG) and proteoglycan composi-
tion. Collagen breakdown would facilitate a higher degree of movement
and stretch in the tissue, which is required for softening. Similarly, an in-
crease in the GAG content of the tissues stimulated by prostaglandin
would result in a decrease in collagen bril agglutination and ultimately
would reduce the stretch resistance of the remaining collagen [20].
Elevation of the GAG hyaluronan is a well known change that facilitates
the degradation of collagen bers and can cause further viscoelasticity
of the cervix. Cervical softening occurs in the weeks or days preceding
childbirth [21]; thus, the cervix can be inverted at this stage without
difculty. Furthermore, owing to the shorter cervix in cases of placenta
previa [22], cervical inversion might be applied even more readily and
successfully.
A case of inversion or invagination of a partly effaced and dilated
cervix into the lower segment at the time of cesarean delivery was
reported by Sivasuriya and Herath [23]. They observed a pouch-like pro-
trusion, identied it as the cervix uteri, and pushed it back to the original
anatomic position without any postoperative complications.
It should be considered that, in any clinical emergency, the staff
needs to perform in stressful conditions. In these situations, high prior-
ity should be given to procedures that can be performed in accordance
with simple instructions and by less skilled staff. The present study
 N. Sakhavar et al. / International Journal of Gynecology and Obstetrics 128 (2015) 122125
has demonstrated that cervical inversion is a simple and effective
technique.
The main limitation of the present study was the small sample size. If
the present observations are conrmed in a larger series, cervical inver-
sion could become part of the routine procedures used to treat women
with placenta previa. Cervical inversion could be used for management
of PPH because it compresses and occludes lower-segment arteries,
leads to relative hemostasis, and provides additional time for suturing
the bleeding site. Furthermore, the procedure is easy to perform and
does not need specialist skills, materials, or equipment; it is a rapid
maneuver that can preserve the uterus and future fertility of women
with placenta previa and placenta accreta/increta.
Conict of interest
The authors have no conicts of interest.
References
[1] Shao Y, Pradhan M. Intrauterine gauze packing in primary post partum hemorrhage
following caesarean section: a clinical study. Nepal J Obstet Gynaecol 2012;7(1):
336.
[2] Jegasothy R. Sudden maternal deaths in Malaysia: a case report. J Obstet Gynaecol
Res 2002;28(4):18693.
[3] Anand AR, Gupta D, Prasad A. Reducing intraoperative lower segment blood loss in
placenta previa with Ashok Anand stitch. Int J Reprod Contracept Obstet Gynecol
2013;2(2):13540.
[4] Lalonde A, Daviss BA, Acosta A, Herschderfer K. Postpartum hemorrhage today:
ICM/FIGO initiative 20042006. Int J Gynecol Obstet 2006;94(3):24353.
[5] Portilla D, Hernndez-Giraldo C, Moreno B, Quijano F, Hoyos LR, Angarita AM, et al. A
local hemostatic agent for the management of postpartum hemorrhage due to
placenta previa and placenta accreta: a cross-sectional study. Arch Gynecol Obstet
2013;288(3):5439.
[6] Wee L, Barron J, Toye R. Management of severe postpartum haemorrhage by uterine
artery embolization. Br J Anaesth 2004;93(4):5914.
[7] Fuglsang K, Petersen LK. New local hemostatic treatment for postpartum hemor-
rhage caused by placenta previa at cesarean section. Acta Obstet Gynecol Scand
2010;89(10):13469.
125
[8] Usta IM, Hobeika EM, Musa AA, Gabriel GE, Nassar AH. Placenta previa-accreta: risk
factors and complications. Am J Obstet Gynecol 2005;193(3 Pt 2):10459.
[9] Oyelese Y, Smulian JC. Placenta previa, placenta accreta, and vasa previa. Obstet
Gynecol 2006;107(4):92741.
[10] Law LW, Chor CM, Leung TY. Use of hemostatic gel in postpartum hemorrhage due
to placenta previa. Obstet Gynecol 2010;116(Suppl. 2):52830.
[11] Matsubara S. Available hemostatic measures for postpartum hemorrhage in rural
settings. Rural Remote Health 2012;12:2248.
[12] Kumru P, Demirci O, Erdogdu E, Arisoy R, Ertekin AA, Tugrul S, et al. The Bakri
balloon for the management of postpartum hemorrhage in cases with placenta
previa. Eur J Obstet Gynecol Reprod Biol 2013;167(2):16770.
[13] Ganguli S, Stecker MS, Pyne D, Baum RA, Fan CM. Uterine artery embolization in the
treatment of postpartum uterine hemorrhage. J Vasc Interv Radiol 2011;22(2):
16976.
[14] Doumouchtsis SK, Papageorghiou AT, Arulkumaran S. Systematic review of
conservative management of postpartum hemorrhage: what to do when medical
treatment fails. Obstet Gynecol Surv 2007;62(8):5407.
[15] Johanson R, Kumar M, Obhrai M, Young P. Management of massive postpartum
haemorrhage: use of a hydrostatic balloon catheter to avoid laparotomy. BJOG
2001;108(4):4202.
[16] Matsubara S, Kuwata T, Usui R, Ohkuchi A. 'Holding the cervix' technique for
post-partum hemorrhage for achieving hemostasis as well as preventing prolapse
of an intrauterine balloon. J Obstet Gynaecol Res 2013;39(5):11167.
[17] Palacios Jaraquemada JM, Garcia Mnaco R, Barbosa NE, Ferle L, Iriarte H, Conesa HA.
Lower uterine blood supply: extrauterine anastomotic system and its application in
surgical devascularization techniques. Acta Obstet Gynecol Scand 2007;86(2):
22834.
[18] Gizzo S, Zambon A, Saccardi C, Patrelli TS, Di Gangi S, Carrozzini M, et al. Effective
anatomical and functional status of the lower uterine segment at term: estimating
the risk of uterine dehiscence by ultrasound. Fertil Steril 2013;99(2):496501.
[19] Landon MB. Predicting uterine rupture in women undergoing trial of labor after
prior cesarean delivery. Semin Perinatol 2010;34(4):26771.
[20] Word RA, Li XH, Hnat M, Carrick K. Dynamics of cervical remodeling during
pregnancy and parturition: mechanisms and current concepts. Semin Reprod Med
2007;25(1):6979.
[21] Timmons B, Akins M, Mahendroo M. Cervical remodeling during pregnancy and
parturition. Trends Endocrinol Metab 2010;21(6):35361.
[22] Ghi T, Contro E, Martina T, Piva M, Morandi R, Orsini LF, et al. Cervical length and risk
of antepartum bleeding in women with complete placenta previa. Ultrasound Obstet
Gynecol 2009;33(2):20912.
[23] Sivasuriya M, Herath HP. Inversion of cervix uteri at caesarean section. Br Med J
1976;1(6012):7467.