FIGO Classification As Submitted

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FIGO classification for the clinical

diagnosis of placenta accreta spectrum


disorders+,§

Eric Jauniaux1, Diogo Ayres-de-Campos2,6, Jens Langhoff-


Roos3, Karin A Fox4, Sally Collins5; FIGO Placenta Accreta
Diagnosis and Management Expert Consensus Panel7

1
EGA Institute for Women’s Health, Faculty of Population Health Sciences,
University College London (UCL), London, UK.
2
Medical School, University of Lisbon, Santa Maria Hospital, Lisbon, Portugal.
3
Department of Obstetrics, Rigshospitalet, University of Copenhagen, Denmark.
4
Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology,
Baylor College of Medicine, Houston, Texas, USA.
4
Nuffield Department of Women’s and Reproductive Health, University of Oxford,
and the Fetal Medicine Unit, John Radcliffe Hospital, Oxford, UK
5
FIGO Safe Motherhood and Newborn Health Committee

The authors report no conflict of interest


+
Promoted by the FIGO Safe Motherhood and Newborn Health Committee;
coordinated by Eric Jauniaux.
§
The views expressed in this document reflect the opinion of the individuals and not
necessarily those of the institutions that they represent.

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Expert Consensus panel:

Dr Greg Duncombe Australia and New Zealand


Dr Philipp Klaritsch Austria
Dr Frederic Chantraine Belgium
Professor John Kingdom Canada
Dr Lene Groenbeck Denmark
Dr Kristiina Rull Estonia
Dr Minna Tikkanen Finland
Professor Loic Sentilhes France
Professor Tengiz Asatiani Georgia
Dr Wing Cheong Leung Hong Kong
Professor Taghreed AIhaidari Iraq
Dr Donal Brennan Ireland
Dr Muhieddine Seoud Lebanon
Professor Ahmed Mahmoud Hussein Egypt
Dr Ravindran Jegasothy Malaysia
Dr Kamal Nusrat Shah Pakistan
Professor Dorota Bomba-Opon Poland
Professor Corinne Hubinont Belgium
Professor Priya Soma-Pillay Republic of South Africa
Asistant Professor Nataša Tul Mandić Slovenia
Dr Pelle Linqvist Sweden
Dr Berglind Arnadottir Sweden
Professor Irene Hoesli Switzerland
Dr Rafael Cortez Venezuela

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1 Irving and Hertig are credited for having published, in 1937, the first cohort study of

2 placenta accreta in the international literature [1]. Their article included

3 comprehensive clinical and histopathologic descriptions of 20 cases and a literature

4 review of 86 cases published before 1935. All their cases were described as

5 ‘adherenta’, which they characterized clinically as a placenta adherent to the uterine

6 wall without easy separation and/or bleeding from the placental bed, and

7 histologically as absence of decidual layer/Nitabuch layer between the placenta and

8 myometrium. These diagnostic criteria were not new at the time and had been in use

9 since the mid-1920s, including by the authors of case reports with histological

10 evidence of villous invasion of the myometrium [2].

11 Predisposing factors identified in the 1920s and 1930s were previous manual

12 removal of placenta and/or “vigorous” uterine curettage. Only one of the 20 patients

13 included in the Irving and Hertig series had a previous caesarean delivery [1].

14 Similarly, in their review of the previous 86 case reports, only one woman had a prior

15 caesarean delivery. Before the development of antibiotics, damage to the uterine wall

16 after uterine curettage or manual removal of the placenta was often aggravated by

17 endometritis. This likely resulted in scar tissue forming focally within the superficial

18 myometrium which is not comparable to the extensive myometrial scar caused by

19 multiple caesarean deliveries [4-6]. The low incidence of full-thickness myometrial

20 scarring may explain why very few cases of invasive placentation were reported before

21 the 1950s, when caesarean deliveries became safer and therefore increasingly

22 common. There is now compelling epidemiological evidence that accreta placentation

23 has become essentially an iatrogenic condition, secondary to the modern era

24 caesarean section epidemic [3,4]. In early pathologic studies, the distribution of

25 placenta creta, increta and percreta was found to be 69.5%, 23.7% and 6.8%,

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26 respectively [3]. The incidence of invasive cases has increased in the last two decades

27 but the data are limited due to wide variation in the methodology used in cohort

28 studies.

29 Placenta accreta was re-defined in the mid-1960’s by Lukes et al. [7] as a

30 spectrum of abnormal placentation disorders. These include placenta adherenta or

31 vera also referred to as placenta creta by pathologists, where the villi are attached

32 directly to the surface of the myometrium without invading it; placenta increta, where

33 the villi penetrate deeply into the myometrium up to the uterine serosa and placenta

34 percreta, where the invasive villous tissue penetrates through the uterine serosa and

35 may reach the surrounding pelvic tissues, vessels and organs. They also showed that

36 different grades of the placenta accreta spectrum (PAS) can co-exist in the same

37 specimens and that an accreta area can be focal or extended (diffuse). This remains

38 the most comprehensive description of placenta accreta published so far, and was

39 largely incorporated in the recent FIGO guidelines [3] and other publications [6].

40 Similarly, to other clinical conditions, histopathology is now widely considered

41 as the gold standard modality recommended to confirm clinical diagnoses but it is

42 often unavailable in adherent accreta or conservatively managed cases, and was not

43 described by the pioneer pathologists of the 19th and early 20th centuries [3]. Moreover,

44 unlike cancer staging, retrospective clinical and/or pathological grading of PAS has no

45 direct long-term impact on the life of women. All these aspects may explain the

46 apparent lack of interest in accurately differentiating between adherent and invasive

47 forms, both by clinicians and pathologists and/or the lack of trained perinatal

48 pathologists in many centres. As a result, the 1920-1930’s criteria, based mostly on

49 adherent cases, continued to be used by several authors of cohort studies. However,

50 this can lead to misleading conclusions, as adherent and invasive accreta placentation

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51 have very different outcomes and require different management. To compound this,

52 although 80-90% of prenatally diagnosed PAS are managed with caesarean

53 hysterectomy [8], around half of the authors fail to report the extent of villous

54 attachment or invasion after peri-partum hysterectomy [9].

55 Recent variants of the classical clinical description of PAS often include criteria

56 such a “difficult manual, piecemeal removal of the placenta”, “absence of spontaneous

57 placental separation 20-30 minutes after birth despite active management, including

58 bimanual massage of the uterus, use of oxytocin and controlled traction of the

59 umbilical cord”, “retained placental fragment requiring curettage after vaginal birth”

60 and “heavy bleeding from the placentation site after removal of the placenta during

61 cesarean delivery” [10-13]. This has resulted in a multitude of different clinical criteria,

62 which can be easily confused with non-accreta placental retention and secondary

63 uterine atony. With so many different criteria all-purporting to represent PAS, but

64 without any attempt to differentiate between adherent and invasive forms, it is

65 unsurprising that there is a wide variation in the reported prevalence over the last 30

66 years.

67 Adding to the confusion is the wide heterogeneity in terminology used to

68 describe the different grades of accreta placentation: these include “placental

69 adhesive disorders”, “abnormal placental adherence”, “advanced invasive

70 placentation” and “abnormal myometrial invasion” [9,14]. A recent popular label used

71 by clinicians reporting on the prenatal diagnosis of PAS has been “morbidly adherent

72 placenta”, which was used in the 19th Century to describe placental retention. It has

73 been recently used by the World Health Organization (WHO) international statistical

74 classification of diseases (ICD-10) (www.who.int/classifications/icd) and has led to

75 some exotic translation such as “the pernicious placenta” recently used by Chinese

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76 authors in both local and international journals [15,16]. This point also highlights the

77 limited impact of accreta placentation research on the general scientific literature, as

78 leading medical journals are unlikely to publish articles on diseases that do not have

79 universally accepted diagnostic criteria and unequivocal terminology. Each of the

80 other terminologies used so far are suboptimal and exclusive as they do not describe

81 the different grades of PAS i.e. "adherent" which does not include the invasive grades

82 increta and percreta and "invasive" which can be confused with gestational

83 trophoblastic disease and in particular invasive intra-uterine choriocarcinoma.

84 Consequences reach far beyond a simple debate on what is the most

85 adequate terminology. So far, the lack of use of standardized clinical criteria for the

86 diagnosis of the condition at birth and the histopathologic differential diagnosis

87 between adherent and invasive accreta placentation has led to wide heterogeneity

88 between studies for all epidemiologic and outcome parameters [18]. Distinguishing

89 between adherent and invasive forms of accreta has a direct impact on the accurate

90 evaluation of epidemiology, on improving the understanding of the underlying

91 pathology, and most importantly on the development of better management

92 strategies. In addition, labelling cases of placenta retention as accreta or morbidly

93 adherent leads to overdiagnosis which can influence treatment decision leading to

94 overtreatment and diagnosis related anxiety for many patients. The process of

95 clarifying the reporting data on placenta accreta in the international literature started

96 recently with the development of a grading system for the clinical diagnosis of PAS

97 [19]. The classification presented in Table 1 was developed from this grading

98 scheme, and reviewed by the members of the FIGO Placenta Accreta Spectrum

99 Disorders Diagnosis and Management Expert Consensus Panel [20]. Of note, it

100 refers to a classification and not staging system, to differentiate it from the

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101 terminology used for cancer. As an example, for the use of the classification, we

102 have summarised the recommendations of the recent FIGO guidelines for the

103 conservative [21] and non-conservative surgical management [22] of PAS according

104 to the grade of accreta invasiveness defined in the present classification (see

105 appendix 1).

106 The accreta placentation process has an impact on both the anatomy of a

107 portion of the placenta and on the anatomy of the surrounding deep uterine circulation

108 [6]. The accreta area will not spontaneously deliver at birth and any attempt in doing

109 so may result in rapidly uncontrollable bleeding from the deep uterine vessels or the

110 neovascularisation in the accreta area. The deeper and larger the accreta area inside

111 the uterine wall, the higher the risks of severe haemorrhagic complications and need

112 to perform an emergency hysterectomy. To avoid unnecessary complex surgical

113 procedure, clinicians should differentiate between placenta percreta and a ‘uterine

114 window’ which is an area of cesarean scar dehiscence with normal placentation

115 underneath (or sometime seen poking through). In the latter, the surrounding uterine

116 tissue appears relatively normal with no neovascularity or placental bulge. If the

117 placenta is eventually delivered manually in whole or in pieces and it is unlikely to have

118 been accreta. The manual removal of a non-accreta retained placenta can also be

119 associated with severe haemorrhage due to secondary uterine atony but in these

120 cases, conservative management techniques such as compressive sutures and

121 intrauterine balloon are often successful in controlling the bleeding. These cases

122 should not be reported as successful management of PAS.

123 It is pivotal to improve the accuracy of PAS diagnosis in the international

124 literature, and for this purpose we also propose reporting guidelines, which include a

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125 standardized basic dataset for future clinical research and to allow comparison

126 between centers with different management strategies (Table 2). This protocol does

127 not replace the general EQUATOR network guidelines, such as the PRISMA guideline

128 for systematic reviews, but rather it serves to elevate the international discourse about

129 PAS to a scientific caliber that matches the gravity of the disease. Adherence to this

130 new FIGO classification will improve future systematic reviews and meta-analysis and

131 provide more accurate epidemiologic data which are essential to improve clinical

132 outcomes.

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REFERENCES

1. Irving C, Hertig AT. A study of placenta accreta. Surgery, Gynecol Obstet.


1937;64:178-200.
2. Forster DS. A case of placenta accrete. Can Med Assoc J. 1927;17:204-7.
3. Jauniaux E, Chantraine F, Silver RM, Langhoff-Roos J; FIGO Placenta
Accreta Diagnosis and Management Expert Consensus Panel. FIGO
consensus guidelines on placenta accreta spectrum disorders: Epidemiology.
Int J Gynaecol Obstet. 2018;140:265-73.
4. Jauniaux E, Jurkovic D. Placenta accreta: pathogenesis of a 20th century
iatrogenic uterine disease. Placenta. 2012;33:244-51.
5. Jauniaux E, Bhide A, Burton GJ. Pathophysiology of accreta. In: Silver, R. ed.
Placenta accreta syndrome. Portland: CRC Press; 2017:13–28.
6. Jauniaux E, Collins SL, Burton GJ. Placenta accreta spectrum:
Pathophysiology and evidence-based anatomy for prenatal ultrasound
imaging. Am J Obstet Gynecol. 2018;218:75-87.
7. Luke RK, Sharpe JW, Greene RR. Placenta accreta: The adherent or invasive
placenta. Am J Obstet Gynecol. 1966;95:660–8.
8. Jauniaux E, Bhide A. Prenatal ultrasound diagnosis and outcome of placenta
previa accreta after caesarean delivery: a systematic review and meta-
analysis. Am J Obstet Gynecol 2017;217:27–36.
9. Jauniaux E, Collins SL, Jurkovic D, Burton GJ. Accreta placentation. A
systematic review of prenatal ultrasound imaging and grading of villous
invasiveness. Am J Obstet Gynecol. 2016; 215:712-21.
10. Gielchinsky Y, Rojansky N, Fasouliotis SJ, Ezra Y. Placenta accreta--summary
of 10 years: a survey of 310 cases. Placenta. 2002;23:210-4.
11. Wu S, Kocherginsky M, Hibbard JU. Abnormal placentation: twenty-year
analysis. Am J Obstet Gynecol. 2005;192:1458–61.
12. Umezurike CC, Nkwocha G. Placenta accreta in Aba, south eastern, Nigeria.
Niger J Med. 2007;16:219-22.
13. Seet EL, Kay HH, Wu S, Terplan M. Placenta accreta: depth of invasion and
neonatal outcomes. J Matern Fetal Neonatal Med. 2012;25:2042-5.

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14. Collins SL, Chantraine F, Morgan TK, Jauniaux E. Abnormally adherent and
invasive placenta: A spectrum disorder in need of a name. Ultrasound Obstet
Gynecol. 2018;51:165-6.
15. McDonald KN. How to prevent septicaemia in cases of morbidly adherent
placenta. BMJ. 1885;1:779-80.
16. Huang S, Xia A, Jamail G, Long M, Cheng C. Efficacy of temporary ligation of
infrarenal abdominal aorta during cesarean section in pernicious
placenta previa. Zhong Nan Da Xue Xue Bao Yi Xue Ban. 2017;42:313-19.
17. Dai MJ, Jin GX, Lin JH, Zhang Y, Chen YY, Zhang XB. Pre-cesarean
prophylactic balloon placement in the internal iliac artery to prevent
postpartum hemorrhage among women with pernicious placenta previa. Int J
Gynaecol Obstet. 2018 Jun 7. doi: 10.1002/ijgo.12559.
18. Jauniaux E, Bunce C, Grønbeck L, Langhoff-Roos J. Prevalence and main
outcomes of placenta accreta spectrum: a systematic review and
metaanalysis. Am J Obstet Gynecol 2019;220: in press.
19. Collins SL, Stevenson GN, Al-Khan A, Illsley NP, Impey L, Pappas L, et al.
Three-Dimensional Power Doppler Ultrasonography for Diagnosing
Abnormally Invasive Placenta and Quantifying the Risk. Obstet Gynecol.
2015;126:645-53.
20. Jauniaux E, Ayres-de-Campos D; for the FIGO Placenta Accreta Diagnosis
and Management Expert Consensus Panel. FIGO consensus guidelines on
placenta accreta spectrum disorders: Introduction. Int J Gynecol Obstet 2018;
140:261-4.
21. Sentilhes L, Kayem G, Chandraharan E, Palacios-Jaraquemada J, Jauniaux
E; FIGO Placenta Accreta Diagnosis and Management Expert Consensus
Panel. FIGO consensus guidelines on placenta accreta spectrum disorders:
Conservative management. Int J Gynaecol Obstet. 2018;140:291-8.
22. Allen L, Jauniaux E, Hobson S, Papillon-Smith J, Belfort MA; FIGO Placenta
Accreta Diagnosis and Management Expert Consensus Panel. FIGO
consensus guidelines on placenta accreta spectrum disorders:
Nonconservative surgical management. Int J Gynaecol Obstet. 2018;140:281-
90.

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Table 1: PAS general classification

GRADE 1 Abnormally adherent placenta (PLACENTA ADHERENTA OR CRETA)


Clinical At vaginal delivery
criteria - No separation with synthetic oxytocin and gentle controlled cord
traction.
- Attempts at manual removal of the placenta results in heavy
bleeding from the placenta implantation site requiring mechanical or
surgical procedures.
If laparotomy is required
- Same as above.
- Macroscopically, the uterus shows no obvious distension over the
placental bed (placental ‘bulge’), no placental tissue is seen invading
through the surface of the uterus, and there is no or minimal
neovascularity.
Histologic - Microscopic examination of the placental bed samples from
criteria hysterectomy specimen shows extended areas of absent decidua
between villous tissue and myometrium with placental villi attached
directly to the superficial myometrium.
- The diagnosis cannot be made on just delivered placental tissue nor
on random biopsies of the placental bed.

GRADE 2 Abnormally invasive placentation (PLACENTA INCRETA)


Clinical At laparotomy
criteria - Abnormal macroscopic findings over the placental bed: bluish/purple
colouring, distension (placental ‘bulge’).
- Significant amounts of neovascularity (dense tangled bed of vessels
or multiple vessels running parallel cranio-caudially in the uterine
serosa.
- No placental tissue seen to be invading through the surface of the
uterus.
- Gentle cord traction results in the uterus being pulled inwards
without separation of the placenta (the ‘dimple’ sign).
Histologic Hysterectomy specimen or partial myometrial resection of the increta area
criteria shows placental villi within the muscular fibres and sometimes in the lumen
of the deep uterine vasculature.
GRADE 3 Abnormally invasive placentation (PLACENTA PERCRETA)
GRADE 3a Limited to the uterine serosa
Clinical At laparotomy
criteria - Abnormal macroscopic findings on uterine surface (as above) and
placental tissue seen to be invading through the surface of the
uterus (serosa).
- No invasion into any other organ, including the posterior wall of the
bladder (a clear surgical plane can be identified between the bladder
and uterus).

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Histologic Hysterectomy specimen showing villous tissue within or breaching the
criteria uterine serosa
GRADE 3b With urinary bladder invasion
Clinical At laparotomy
criteria - Same as 3a.
- Placental villi are seen to be invading into the bladder but no other
organs.
- Clear surgical plane cannot be identified between the bladder and
uterus.
Histologic hysterectomy specimen showing villous tissue breaching the uterine serosa
criteria and invading the bladder wall tissue or urothelium.
GRADE 3c With invasion of other pelvic tissue/organs
Clinical At laparotomy
criteria - Same as 3a.
- Placental villi are seen to be invading into the broad ligament,
vaginal wall, pelvic sidewall or any other pelvic organ (+/- invasion of
bladder).
Histologic Hysterectomy specimen showing villous tissue breaching the uterine
criteria serosa and invading pelvic tissues/organs.
NB: For the purposes of this classification, ‘uterus’ includes the uterine body and
uterine cervix.

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Table 2: Basic dataset for PAS reporting.

Background population

1. Institution-based study:
• Display referred cases and cases from local catchment area in separate data
sets.
• Description of background population and cases including number of births,
mode of delivery, parity, local CD rate (stratified by numbers of prior deliveries
and numbers of prior CD).

2. Regional/network/national-based study:
• Description of local background population including number of births, mode
of delivery, parity, CD rates (stratified by numbers of prior deliveries and
numbers of prior CD) for referred cases and local cases.

Description of standardized criteria used for prenatal diagnosis:


• Ultrasound signs of PAS including placental location.
• MRI signs of PAS including surface area and depth.

Management strategy:
• Intended mode of management: vaginal delivery, scheduled CD,
hysterectomy (primary or delayed), focal myometrial resection, leaving the
placenta in situ.
• Actual mode of management: vaginal delivery, scheduled CD, emergent
CD, focal myometrial resection, hysterectomy (primary or delayed), leaving
the placenta in situ.

Confirmation of diagnosis:
• Clinical diagnostic criteria and confirmed histopathological diagnosis when
possible.
• The final diagnosis (clinical, histopathological) should be clearly stated and
made according to the classification in Table 1.

CD= caesarean delivery; MRI= magnetic resonance imaging.

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Appendix 1: Example of Management for PAS using the new classification
presented in table 1. The content of this table is based on the recommendations of
the recent FIGO guidelines for the conservative [20] and non-conservative surgical
management [21] and may need to be adapted to local need and access to
specialised unit/multidisciplinary team.

FOCAL OR DIFFUSE GRADE 1 ANYWHERE IN THE UTERUS


Manual extraction of the placenta may be attempted if a distinct cleavage plane is
found, followed by treatment of postpartum haemorrhage, if necessary with
haemostatic stiches in placental bed or tamponade applied to the placental bed eg
with an intra-uterine balloon. Hysterectomy may be reserved for ongoing bleeding,
should conservative maneuvers fail.

FOCAL GRADE 2 or 3a OUTSIDE THE LOWER UTERINE SEGMENT


Local resection of accreta area and overlying uterus may be attempted, if the
operator is certain that there is no placental invasion into the cervix or parametria.
With abundant or persistent haemorrhage, mechanical or surgical measures to
control haemorrhage may be required, including peri-partum hysterectomy.

DIFFUSE GRADE 2 ANYWHERE IN THE UTERUS or 3a OUTSIDE THE LOWER


UTERINE SEGMENT
Intraoperative ultrasound should be used to locate the placental bed and avoid
transecting it in the uterine incision, if the exact location of the placenta is uncertain.
After fetal extraction, avoid attempts to remove the placenta, ligate and cut the cord
near its placental insertion. Close the hysterotomy and review haemostasis.
If not bleeding; manage according to the patient’s wishes and the experience
of the surgical team with either peri-partum hysterectomy or leaving the placenta in
situ (conservative management). Conservative management can be either the
definitive management or for just a short time until a secondary hysterectomy can
be performed by a more experienced team i.e. with interventional radiology.
If massive or persistent haemorrhage, mechanical or surgical measures to
control haemorrhage are urgently required, with rapid recourse peri-partum
hysterectomy.

GRADE 3 or 3a IN LOWER UTERINE SEGMENT (with prenatal diagnosis)


Consider placement ureteral stents and instilling 100 ml of saline with coloured
agent into bladder. Consider a median infra-umbilical or a wide transverse (e.g.
modified Maylard or a Joel Cohen) skin incision (with vertical fascial incision if
required).
Upon opening the abdomen, a full assessment of the extent of invasion
throughout the pelvis should be made including visualization of the pelvic side
walls which may require opening the broad ligament to aid inspection.
Intraoperative ultrasound should be used to locate the placental bed and avoid
transecting it in the uterine incision. After fetal extraction avoid attempts to remove
the placenta, ligate and cut the cord near placental insertion. Uterotonic agents
should not be used if conservative management is planned and should only be
considered if partial separation of the placenta has resulted in bleeding and the

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operating team feel that increased uterine contraction may reduce blood loss
during the definitive surgery. Close the hysterotomy and review haemostasis.
If no heavy bleeding, manage according to the anticipated complexity of any
surgical management considering the experience of the surgical team and patient’s
wishes and then proceed to either peri-partum hysterectomy or leaving the placenta
in situ (conservative management). Conservative management can be either the
definitive management or for just a short time until a secondary hysterectomy can
be performed by a more experienced team. If there is invasion of the urinary bladder
(3b or 3c) and proceeding to peri-partum hysterectomy,deliberate partial
cystectomy may be required.
If massive or persistent heavy haemorrhage; mechanical or surgical measures
to control hemorrhage are urgently required, with rapid recourse peri-partum
hysterectomy.

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