REVIEW

Antepartum haemorrhage haemorrhage. The report does not distinguish the women who
presented with APH, but three women were diagnosed with
placental abruption and placenta praevia.
Nadia Amokrane The aim of this review is to define causes of APH and discuss
E R F Allen management in accordance with recent guidelines and published
evidence. The MBRRACE-UK report reminds us that APH and
Anna Waterfield PPH are not only important causes of maternal mortality but also
Shreelata Datta of maternal and perinatal morbidity. Therefore the early recog-
nition and management of women presenting with genital tract
blood loss is an important aspect of antenatal assessment. It is
Abstract essential that the obstetrician be prepared for potential sequelae,
Antepartum haemorrhage (APH) is bleeding from or into the genital and thorough antenatal, intrapartum, and postpartum planning
tract occurring between 24 þ 0 weeks’ gestation until birth. It compli- is required.
cates 3e5% of pregnancies. The 2006e2008 report of the Confidential
Enquiries into Maternal Deaths in the UK (CMACE) reported APH as
Causes of APH
the cause of death in four women. The high prevalence of APH, and
its associated perinatal mortality and morbidity makes a thorough un- Cervical and vaginal causes
derstanding of APH is essential for the practising obstetrician. The A common cause of APH is bleeding from the cervix. A cervical
objective of this review is to consider the most common causes of ectropion or ‘erosion’ is where the columnar epithelium that
APH (placenta praevia, placental abruption and local causes), together lines the cervical canal protrudes further onto vaginal surface of
with their management. the cervix. This is more common in pregnancy, and is thought to
be related to high oestrogen levels. The tissue of the ectropion is
Keywords antepartum haemorrhage; obstetric haemorrhage;
very friable and contact bleeding can occur, usually at sexual
placenta accreta; placenta praevia; placental abruption
intercourse or even on passing hard stools. Ectropion can be
easily diagnosed on speculum examination of the cervix.
Cervicitis (inflammation or infection of the cervix) may be an
Introduction
under-diagnosed cause of bleeding in pregnancy and may be
Bleeding in pregnancy is a common reason for presentation to caused by sexually transmitted infections (STIs) such as chla-
labour wards, maternity triage units, GP surgeries and early mydia and gonorrhoea, which can present with abnormal vaginal
pregnancy centres in the UK. bleeding. A high vaginal swab and screening for STIs should be
The management of bleeding in pregnancy varies according to undertaken. Treatment of STIs presenting in pregnancy is
gestation. In this review we specifically address antepartum important, as they can be associated with preterm labour and
haemorrhage (APH) which is defined as bleeding from the genital neonatal morbidity. Bleeding or spotting can also occur from the
tract that occurs from viability onwards, defined here as greater vagina and vulva secondary to non-sexually transmitted in-
than 24 weeks’ gestation. Obstetricians may see women with fections such as thrush, folliculitis, and from trauma.
genital tract bleeding from 16 to 23 weeks’ gestation however Benign cervical polyps are a further cause of APH. If the
management of this group of women may differ. bleeding does not clinically compromise the mother or fetus, and
APH and post-partum haemorrhage (PPH) are the leading the polyp appears non-suspicious then these should not usually
causes of maternal death worldwide. In the UK, maternal deaths be removed in pregnancy.
have continued to decrease. The recent MBRRACE-UK report Cervical carcinoma presenting in pregnancy is uncommon
published in December 2014 showed that maternal mortality in and a detailed history at booking appointment should assess a
the UK had decreased from 11:100, 000 women between 2006 woman’s smear history and history of previous cervical treat-
and 2008 to 10:10,000 between 2009 and 2012. Between 2009 ments. If a cervical carcinoma is suspected on assessment of the
and 2012, 17 mothers in the UK and Ireland died due to cervix then urgent referral to colposcopy is indicated.

Placental causes
Placental abruption: abruptio placenta is the premature sepa-
Nadia Amokrane MBChB is a Specialist Registrar in Obstetrics and ration of a normally sited placenta from the uterus. Placental
Gynaecology at King’s College Hospital, London, UK. Conflicts of abruption can lead to maternal and fetal complications, and ul-
interest: none declared.
timately mortality. Bleeding occurs when the placenta starts to
E R F Allen MBBS BSc MRCOG is a Locum Consultant Obstetrician and separate from the decidua basalis. The presentation of placental
Gynaecologist at King’s College London (PRUH), London, UK. abruption usually includes pain (50%) and bleeding (70e80%)
Conflicts of interest: none declared. however, a concealed abruption (20% of cases) can present with
Anna Waterfield MRCOG is a Senior House Officer in Obstetrics and no pain or bleeding. Premature labour is seen in nearly a third of
Gynaecology at King’s College Hospital, UK. Conflicts of interest: cases of abruption, however, the contraction pains may be
none declared. atypical in nature, with the patient describing severe unremitting
Shreelata Datta MBBS LLM BSc (Hons) MRCOG is a Consultant pain.
Obstetrician and Gynaecologist at King’s College Hospital, London, The incidence of placental abruption is reported between
UK. Conflicts of interest: none declared. 0.26% and 0.80% in literature depending on the type of study

OBSTETRICS, GYNAECOLOGY AND REPRODUCTIVE MEDICINE --:- 1 Ó 2016 Published by Elsevier Ltd.

Please cite this article in press as: Amokrane N, et al., Antepartum haemorrhage, Obstetrics, Gynaecology and Reproductive Medicine (2016),
http://dx.doi.org/10.1016/j.ogrm.2015.11.009
 REVIEW

and population. The biggest risk factor for abruption is a previ- suggest that transvaginal scanning in suspected placenta praevia
ous abruption with a 10-fold increased risk of abruption if there cases is unsafe.
has been an abruption in the previous pregnancy. The risk in- Women with a low-lying placenta at 20 weeks should be
creases to nearly 25% if a woman has had two previous followed up in the third trimester, usually at 32e36 weeks.
abruptions. However, if women have had a previous Caesarean section and
Although there is no single aetiology for placental abruption, a have a low-lying placenta, then a placenta accreta should be
number of risk factors have been identified. These include hy- suspected. If major placenta praevia is suspected in the third
pertension and pre-eclampsia. Notably, when examining risk trimester, then this significantly raises the risk of morbidity and
factors in a control population, chronic hypertension has a preterm delivery. However the diagnosis of placenta praevia
stronger association with abruption (OR 3.13) than pre- should be considered in any patient who presents with painless,
eclampsia (OR 1.73). Smoking is associated with a 90% in- fresh vaginal bleeding or bleeding after intercourse.
crease in the risk of abruption. There is a three-fold increased The most likely symptom from a placenta praevia is painless
risk in pregnancies complicated by prolonged rupture of mem- bleeding in contrast to abruption where pain is likely to co-
branes (PROM). Cocaine use has also been linked to a higher rate present. The bleeding is usually fresh, red and the amount of
of placental abruption. However, despite numerous risk factors APH can vary. The patient may also present with fresh bleeding
and associations, abruption is usually an unexpected event and in early labour, with the onset of labour and cervical dilatation
the vast majority will occur in low risk pregnancies. triggering the bleed or vice versa.

Placenta praevia, placenta accreta, increta and placenta per- Other causes
creta: placenta praevia is the insertion of the placenta partially or Uterine rupture: uterine rupture is a rare event that is defined as
entirely within the lower segment of the uterus after 32 weeks. If loss of the full thickness of the uterine wall integrity. It usually
the placenta does not cover the internal os then it is described as occurs during labour in a woman with a previous Caesarean
a minor praevia and if it partially or fully covers the os then it is section or myomectomy. Within this group the risk is still small;
classified as a major praevia. A morbidly adherent placenta such the incidence of uterine rupture has been estimated at 7 per
as a placenta accreta, increta or percreta invades through the 10,000 planned vaginal births after Caesarean section. Uterine
decidua basalis. In placenta accreta the chorionic villi attach to rupture may present with CTG abnormalities, pain or APH. Early
the myometrium. In placenta increta the placenta has invaded recognition and quick stabilisation of the mother and baby is
into the myometrium; in placenta percreta the placenta invades required as mortality and morbidity is high.
through the myometrium and breaches the uterine serosa.
Placenta percreta may then invade other organs such as the Vasa praevia: vasa praevia is a rare obstetric complication where
bladder. fetal blood vessels cross the internal cervical os. As the incidence
The incidence of low-lying placenta can be up to 28% at the is rare (between 1 in 2000 and 1 in 6000 pregnancies) it is not
routine 20 week anomaly ultrasound scan, but the majority of currently screened for during routine ultrasound. The risk of APH
these will have migrated higher by the following scan, usually at mainly comes with rupture of the membranes or labour, as a
32 weeks or later. The incidence of true placenta praevia at term direct consequence of tearing of the blood vessels. The fetus can
is approximately 3%. be comprised quickly and management if diagnosed or suspected
There are several hypotheses about the aetiology of placenta is usually by immediate category 1 Caesarean section.
praevia. One theory is that the position of the placenta depends
on the site of implantation of the discoid trophoblast when the Unexplained APH
pregnancy is developing and from where the placenta will arise. Some women will present with bleeding that cannot be attributed
A further theory postulates that areas of deficient endometrium to any of the above causes. The RCOG Greentop Guideline ref-
from procedures such as caesarean sections, surgical manage- erences a number of studies over the last four decades that
ment of miscarriage and myomectomies may affect how the demonstrate that pregnancies with unexplained APH are at
placenta attaches in these cases. higher risk of preterm birth and stillbirth. A recent retrospective,
The risk factors for placenta praevia include multiparity, observational study noted that pregnancies complicated by APH
increasing maternal age, smoking, previous praevia and surgical of unknown aetiology are at a higher risk of preterm birth, lower
procedures that may result in deficient endometrium (Table 1). birthweight, induction of labour, and neonatal unit admissions.
The number of previous Caesarean sections also increases the Repeated presentations with unexplained APH in pregnancy
risk of placenta praevia. should raise suspicion and the pregnancy should be monitored as
In well-resourced settings such as in the UK, the majority of high risk, with the need for additional ultrasound scans for fetal
placenta praevia cases may be picked up on ultrasound scan at growth.
20 weeks. Currently the UK National Screening Committee does Healthcare providers should be aware that maternal trauma,
not recommend screening for placenta praevia however, along- including domestic violence, can result in APH, possibly from
side the RCOG, they support most local practice of identifying placental abruption. A third of domestic violence is known to
women by ultrasound whose placenta lies near the internal os at start or escalate in pregnancy. A retrospective study of 2070
the routine 20 week scan. Evidence shows that at the second women subjected to physical violence in pregnancy found an
trimester scan about 26e60% of women with a low lying increased odds ratio of APH in this cohort, compared with con-
placenta on abdominal ultrasound would be reclassified with a trols, of 3.79 (95% CI 1.38e10.40). Women who present with
more accurate transvaginal scan. There have been no reports to

OBSTETRICS, GYNAECOLOGY AND REPRODUCTIVE MEDICINE --:- 2 Ó 2016 Published by Elsevier Ltd.

Please cite this article in press as: Amokrane N, et al., Antepartum haemorrhage, Obstetrics, Gynaecology and Reproductive Medicine (2016),
http://dx.doi.org/10.1016/j.ogrm.2015.11.009
 REVIEW

multidisciplinary team including a senior obstetrician, anaes-

Risk factors for placenta praevia thetist, and senior midwife. Input is also frequently required
Risk factors from blood transfusion technicians, haematologists, neo-
natologists, and porters. Obstetric units will usually have fixed
Placenta praevia Large placental area protocols for the management of massive obstetric haemorrhage
(multiple pregnancy) that should be activated if a woman presents with or develops
Advanced maternal age massive haemorrhage. These protocols should be actively
High parity rehearsed in annual skills training in order to prepare for such
Uterine scar (caesarean section, cases.
myomectomy) The RCOG Greentop Guideline defines the severity of APH, as
Previous placenta praevia outlined in Table 2. However, it should be remembered that the
Smoking, cocaine use amount of blood lost can be underestimated, particularly as the
Placental pathology amount of blood seen on vaginal examination may not be an
Placental abruption Previous placental abruption accurate representation of the total blood lost.
Hypertension The initial assessment of a woman with APH should include
Pre-eclampsia the ABC approach to stabilise the patient (Table 3) and assess the
Smoking, cocaine use total estimated blood loss. However, it is important to remember
Premature rupture of membranes that not all blood loss is revealed, so the clinical features of blood
Coagulopathies loss are extremely important (e.g. grade of shock) to formulating
Multiple gestation appropriate management plans.
Advanced maternal age Patients with major or massive obstetric haemorrhage should
Abdominal trauma be managed in left lateral tilt to reduce hypotension secondary to
Vasa praevia Velamentous insertion of umbilical cord uterine compression of the inferior vena cava. Resuscitation and
Succenturiate, bilobe placenta stabilization of the mother is the key priority. Following the
Multiple gestation initial survey and after commencing resuscitation, the cause and
IVF pregnancy extent of the APH should be assessed by history taking and
Uterine rupture Multiparity carrying out a full examination.
Congenital uterine anomalies Abdominal examination may illicit a ‘woody’ or tense uterus,
Uterine scar (secondary to caesarean which is characteristically seen in placental abruption or it may
section, myomectomy etc) show the patient is contracting and could be in labour. If a pa-
Maternal age tient with known placenta praevia presents with bleeding, then a
Abnormal placentation digital examination or speculum examination is not necessary. A
Uterine distension (multiple gestation, digital examination or speculum may be indicated where
polyhydramnious, macrosomia) placenta praevia has been excluded to check for a cause for the
Gestation >40 weeks APH and to assess cervical dilatation. The diagnosis of vasa
Uterine rupture Obstructed labour praevia should be considered when the APH has been associated
with rupture of membranes.
Table 1
Investigations
APH and other signs suggestive of domestic violence or, who The RCOG guideline recommends that all patients with APH
disclose violence, should be identified and managed appropri- should have a full blood count (FBC) and a group and save. A
ately by a multidisciplinary team who have been specially Kleihauer test is also necessary for all Rhesus negative women.
trained in domestic violence to safeguard pregnant women. Women who present with major or massive haemorrhage should
also have liver and renal function blood tests and a coagulation
Diagnosis and management of APH screen including fibrinogen. They also may benefit from a
bedside blood check such as a Hemacue since the FBC may not
Women who present with major haemorrhage and signs of give an accurate immediate estimate of blood loss.
shock should be seen in a maternity unit with involvement of a

RCOG definition of APH severity

Description Blood volume

Spotting Staining, streaking or blood spotting noted on underwear or sanitary protection

Minor haemorrhage Blood loss less than 50 ml that has settled
Major haemorrhage Blood loss of 50e1000 ml, with no signs of clinical shock
Massive haemorrhage Blood loss greater than 1000 ml and/or signs of clinical shock

Table 2

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Please cite this article in press as: Amokrane N, et al., Antepartum haemorrhage, Obstetrics, Gynaecology and Reproductive Medicine (2016),
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 REVIEW

Resuscitation pathway for major APH

Assessment Management

A(irway) Check patency

B(reathing) Respiratory rate
Oxygen saturations
10e15L via non rebreathing mask
C(irculation) Heart rate
Capillary refill time
Blood pressure
IV access (consider x 2 16 gauge cannulas)
IV fluid resuscitation crystalloid/colloid/blood
Assess blood loss
Consider catheterisation (input/output monitoring)
D(isabilty) Glasgow coma score
E(xposure) Abdominal examination
Speculum
Vaginal examination
F(etus) CTG Method used gestation dependent
Auscultation FHR
Ultrasound

Table 3

Even with bedside haemoglobin checks and laboratory FBC, it be hospitalised until elective delivery although there is no evi-
should be noted that after acute major blood loss these tests can dence to support this. In accordance with the RCOG Green-top
be misleading during or soon after the initial haemorrhage. guideline, women with placenta praevia in the third trimester
Therefore, initial diagnosis and management of APH should be should be counselled about the risks of preterm delivery and
based on clinical criteria and observations. obstetric haemorrhage. The place and package of care should be
After stabilizing the mother, the fetal heart rate should be individualised to meet the needs of each patient. If care is at
checked. There is no clear guidance or evidence to support home, the woman should be within close proximity to the hos-
monitoring fetuses during APH as there may be transient ab- pital, have a constant companion at home, and be aware of when
normalities with the CTG. Clinical judgement is essential to make she should attend hospital immediately.
a decision regarding mode and timing of delivery based on likely
diagnosis and the maternal and fetal status. For example, if an Blood products
abruption is suspected and there is an abnormal CTG then the Managing severe antepartum haemorrhage frequently requires
CTG findings are likely to be associated with fetal hypoxia and so blood transfusion and considering delivery with surgical in-
delivery would be indicated for fetal benefit. terventions to arrest the bleeding. If women require blood
Ultrasound can be used to determine placental site, or to transfusion then individually cross-matched blood is ideal.
check fetal growth, liquor and Doppler studies once the bleeding Rarely, if blood loss is so excessive that the processing time for
has settled. It is not recommended as a diagnostic tool to di- this would be clinically unacceptable then Group O Rhesus
agnose abruption as the reported sensitivity is only between 25 negative red cells should be utilised. Commencing red cell
and 50%. transfusion is based on clinical evaluation and haematological
Generally most clinicians currently do not recommend tocol- investigations, if available. If a coagulopathy develops then fresh
ysis if a patient is actively bleeding. The RCOG recommends a frozen plasma (FFP) should be administered before one blood
single course of steroids between 24 and 34 weeks if delivery is volume is lost. Haematological investigation and specialist
likely to be preterm. advice should guide the further use of FFP, cryoprecipitate, and
platelets in massive obstetric haemorrhage. The RCOG Green-top
Conservative management of placenta praevia guideline on blood transfusion in obstetrics advises that cry-
Women with placenta praevia were previously advised to remain oprecipitate may be indicated when there is bleeding with
as inpatients from 34 weeks until elective delivery. Currently fibrinogen concentration below 1 g/L. The platelet count should
there is limited evidence to support either hospital-based or be maintained at above 75  109/L.
home-based care in the third trimester. Women with placenta It is important that women who will refuse blood products in
praevia who have APH that resolves spontaneously without an emergency, including Jehovah’s witnesses, are identified in
requiring immediate delivery are likely to remain in hospital until the antenatal period and referred to consultant-led care. These
bleeding has completely ceased. With recurrent APH in the third women are at higher risk of morbidity and mortality in the case
trimester for any pathology, it is common practice for patients to of APH. The healthcare provider and patient should discuss what

OBSTETRICS, GYNAECOLOGY AND REPRODUCTIVE MEDICINE --:- 4 Ó 2016 Published by Elsevier Ltd.

Please cite this article in press as: Amokrane N, et al., Antepartum haemorrhage, Obstetrics, Gynaecology and Reproductive Medicine (2016),
http://dx.doi.org/10.1016/j.ogrm.2015.11.009
 REVIEW

blood components and blood derivatives (for example clotting audits and reviews are imperative for individual units to learn
factor concentrates) would be acceptable to the woman in the through previous experiences and near-misses. All maternity
event of serious blood loss, and also if autologous transfusion in multidisciplinary team must be regularly updated in their ob-
the form of cell salvage can be used. There should be a signed stetric haemorrhage protocols e both antenatal and post-
advanced directive and all discussions clearly documented. partum. A
Antenatally, any woman who would refuse blood transfusion or
blood products should have their haemoglobin levels optimised.
FURTHER READING
In the event of major APH or indeed PPH, a consultant obste-
Antepartum haemorrhage RCOG Green top guideline 63. 2011,
trician, anaesthetist and haematologist should be informed. If a
https://www.rcog.org.uk/globalassets/documents/guidelines/gtg_
woman who would refuse donor blood is diagnosed antenatally
63.pdf.
with placenta accreta or this is suspected, it is recommended that
Anath CV, Savitz DA, Williams MA. Pracental abruption and its asso-
delivery is planned in a facility with access to interventional
ciation with hypertension and prolonged rupture of membranes: a
radiology. There is insufficient evidence on whether prophylactic
methodologic review and meta-analysis. Obstetrics Gynecol 1996
catheter placement for balloon occlusion or embolisation is
Aug; 88: 309e18.
advantageous.
Blood transfusions in Obstetrics RCOG Green top guideline 47.
Delivery techniques and post-partum care https://www.rcog.org.uk/globalassets/documents/guidelines/
Placental abruption and placenta praevia can lead to ongoing gt47bloodtransfusions1207amended.pdf.
bleeding after delivery. Bleeding should be managed according to Knight M, Kenyon S, Brocklehurst P, et al., eds. on behalf of
normal post-partum haemorrhage protocols, with uterotonic MBRRACEUK. Saving lives, improving mothers’ care e lessons
agents and surgical interventions such as intrauterine balloons, learned to inform future maternity care from the UK and Ireland
B-Lynch suture, uterine artery embolization and hysterectomy as confidential enquiries into maternal deaths and morbidity 2009e12.
required. In cases of placenta accreta managed by Caesarean Oxford: National Perinatal Epidemiology Unit, University of Oxford,
section, where the placenta fails to separate, managament op- 2014.
tions include leaving it in situ and proceeding to either elective Neilson JP. Interventions for suspected placenta praevia. Cochrane
hysterectomy or conservative management. There are no rand- Database Syst Rev 2003 (2):CD001988.
omised control trials to compare approaches directly but case Neilson JP. Interventions for treating placental abruption. Cochrane
series show successful outcomes with both approaches. If the Database Syst Rev 2003 (1):CD003247; reviewed 2009.
placenta is left in situ and the uterus is spared, conservative Royal College of Obstetricians and Gynaecologists. Placenta praevia,
management involves prophylactic antibiotics and lengthy placenta praevia accreta and vasa praevia: diagnosis and man-
follow-up with beta-HCG measurement and imaging to ensure agement. Green-top Guideline No. 27. London: RCOG, 2011.
resolution. Women should be warned of the risk of persisting Royal College of Surgeons. Code of practice for management of Je-
bleeding and infection. hovah witnesses. London: IBSA Press, 2002.
Tikkanen M, Nuutila M, Hiilesmaa V, et al. Clinical presentation and risk
Conclusion factors of placental abruption. Acta Obstetricia Gynecol Scand
2006; 85: 700e5. http://dx.doi.org/10.1080/00016340500449915.
APH can be a traumatic and concerning event for women in Toivonen S, Heinonen S, Anttila M, et al. Reproductive risk factors,
pregnancy. Early recognition and management is therefore vital, Doppler findings, and outcome of affected births in placental
together with a relevant postnatal debrief. The MBRRACE-UK abruption: a population-based analysis. Am J Perinatol 2002; 19:
report highlights that haemorrhage is still a significant contrib- 451e60.
utor to UK maternal morbidity and mortality. Therefore, local

OBSTETRICS, GYNAECOLOGY AND REPRODUCTIVE MEDICINE --:- 5 Ó 2016 Published by Elsevier Ltd.

Please cite this article in press as: Amokrane N, et al., Antepartum haemorrhage, Obstetrics, Gynaecology and Reproductive Medicine (2016),
http://dx.doi.org/10.1016/j.ogrm.2015.11.009