European Journal of Obstetrics & Gynecology and Reproductive Biology 159 (2011) 255260

Contents lists available at ScienceDirect

European Journal of Obstetrics & Gynecology and

Reproductive Biology
journal homepage: www.elsevier.com/locate/ejogrb

Review

Secondary post-partum haemorrhage: challenges in evidence-based causes

and management
Isaac A. Babarinsa a,*, Richard G. Hayman a, Tim J. Draycott b
a
The Womens Centre, Gloucestershire Hospitals NHS Trust, Gloucester GL1 3NN, United Kingdom
b
Womens Health Directorate, Southmead Hospital, Bristol, United Kingdom

A R T I C L E I N F O A B S T R A C T

Article history: Secondary postpartum haemorrhage (SPPH) is an important post-natal issue, whose signicance is
Received 15 February 2011 perceived differently between practices, settings and probably within cultures.
Received in revised form 7 July 2011 It is generally less focussed upon, in contrast to its primary counterpart.
Accepted 14 July 2011
Patients prefer that it is treated promptly, even when it is not life-threatening. Intensity of blood loss,
and the lesser popularity of conservative management drive clinicians towards the active options.
Keywords: Remarkably, none of the current treatment options is based on any evidence. Suction evacuation of
Delayed postpartum haemorrhage
the uterus may be complicated by life-threatening complications and blood transfusion. There are a few
Retained products of conception
Pelvic ultrasound scan
guidelines, and probably no protocols. In this review, we highlight salient factors to take into
Suction evacuation consideration, and propose a locally adaptable owchart, which may be of use to General Practice
Uterotonics doctors, Community Midwives and Obstetricians.
Subinvolution 2011 Elsevier Ireland Ltd. All rights reserved.

Contents

1. Introduction and denition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 255

2. Epidemiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 255
3. Patient perception . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256
4. Presumed and documented causes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256
4.1. Investigations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257
4.2. Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257
5. Prediction and recurrence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 258
6. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 259
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 259

1. Introduction and denition 2. Epidemiology

Any signicant bleeding from the genital tract 24 h after The frequency of SPPH is difcult to estimate. Hospital-based
childbirth, by any route, may be dened as a Secondary Post- gures may only reect severe SPPH, or a self-selected group of
Partum Haemorrhage (SPPH). It has also been variously referred to patients who by-pass their primary care givers.
as: delayed post-partum haemorrhage, prolonged postpartum Boyd et al. [1] report that 0.2% of women who delivered in two
haemorrhage or prolonged heavy lochia. SPPH would appear to be US hospitals were re-admitted for SPPH. An on-line review [2],
an important post-natal problem seen more often by the General estimated that SPPH occurs in 12% of women.
Practitioner (GP), Community Midwife or Emergency Room It would appear that clinicians generally have inadequate
Physician. knowledge of the pathophysiology of the postpartum period and
consequently sub-optimally manage its complications [3]. For
example, after quoting a statement from the most widely used
obstetric textbook in the United States, Visness et al. [4] observe
* Corresponding author. Tel.: +44 8454225508; fax: +44 08454226105. that there were no scientic references or empirical data to support
E-mail address: Isaac.babarinsa2@glos.nhs.uk (I.A. Babarinsa). the contention that, the retention of small portions of the placenta or

0301-2115/$ see front matter 2011 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.ejogrb.2011.07.029
256 I.A. Babarinsa et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 159 (2011) 255260
imperfect involution of the placental site may explain persistence of
lochia for more than 2 weeks.
An important (but seldom cited) study in Israel [5] identied
three patterns of lochial blood loss:
 Type I: rubra ! serosa ! alba; with equal duration of each phase
 Type II: rubra ! serosa ! alba; with a prolonged rubra phase
and
 Type III: rubra ! serosa/alba ! rubra ! serosa.
The second wave of lochial blood loss in the 3rd group, lasted
almost twice the duration of the rst and occurred between the
14th and postpartum 28th day. But more importantly, the amount
gradually reduced from moderate to scant, irrespective of the colour
type.
Could this be the entity we most frequently and conveniently
label as SPPH and treat so aggressively?
Nearly a third of women with von Willebrand disease in one
report [6] had SPPH which was noted to be intermittent,
occasionally prolonged, and frequently requiring blood transfu-
sion. In a recent prospective study of the duration of lochia
amongst 115 postpartum women in London, up to a third reported
losses beyond six weeks following delivery [7]. There were no
statistical differences between those women with and those
without inherited coagulopathies.
3. Patient perception
In a random sampling of 1249 recently delivered women in
Aberdeen, Scotland with self-reported symptoms [8], more
than three-quarters of those who required re-admission had
either SPPH or pelvic sepsis. Unfortunately, the authors did
not detail the nature of the treatment for SPPH the patients
received.
In 2005 Babarinsa et al. [9] conducted a small community
survey on womens perception of lochial bleeding in a Scottish
county. It was concluded that probably the most important
aspect of the symptomatology of SPPH is the impression the
healthcare provider has about the volume or intensity of blood
loss. The BLiPP study [10] had shown that the frequency of
change of menstrual pads might not necessarily be related to
volume of blood loss reported; almost a third of primipara
reported being shocked by the large amount of blood loss they
experienced.
Up to 9.5% of women in another Aberdeen study, who had
avoided resumption of sexual intercourse up to 8 weeks after
childbirth, mentioned still bleeding as a contributory factor [11].
Table 1
Causes of SPPH: Traditional and Suggested Listing.
Traditionala
Abnormalities of placentation
Idiopathic subinvolution of the uteroplacental vessels
Retained placental tissue
Placenta accrete, increta or percreta
Congenital coagulopathies
Infection
Endometritis
Infection and dehiscence of caesarean section scar
Pre-existing uterine pathology
Submucous broids
Carcinoma of the cervix
Trauma
Rupture of vulval haematoma
a
Adapted from: Neill and Thornton [12].
4. Presumed and documented causes
Table 1 attempts to summarise the causes of SPPH, building
upon an earlier review by Neill and Thornton [12]. The commonest
presumed cause of SPPH is infection, specically endometritis. A
prospective study of the bacteriology of endometrial culture at
caesarean section, repeated at 35 days post-operatively, demon-
strated a 15% sub-clinical endometritis rate [13].
The term sub-involution is not new and describes the nding
of a uterine symhysio-fundal height that had not resolved towards
its pre-pregnancy size. It is now believed that sub-involution of the
placental site is an important contributor to SPPH, as histological
examination of specimens showed large patent dilated supercial
myometrial vessels typically clustered with little intervening
myometrial tissue [14].
Expanding upon this, Khong and Khong [15] observed, in a
review of 169 specimens of curettings submitted for SPPH, that
subinvolution of the placental bed was characterised by widely
distended and patent residua of uteroplacental arteries with only
partial occlusion by thrombosis.
The contraction of adjacent myometrial bres adjacent to blood
vessels have been described as living ligatures in response to
oxytocics which prevents atonic PPH. There is therefore, a possible
role for oxytocics in the management of SPPH, before, or instead of
surgical management.
Retained products of conception may be present following
difculty in placental delivery, the adherence of a placental
cotyledon or the occasional retention of a succenturiate lobe.
In 83 women who had SPPH at Queen Mary Hospital in Hong
Kong, 36% had histologically conrmed retained products of
gestation; over 50% had no febrile illness and over 92% had
multiple courses of antibiotics even though endocervical swabs
were positive in only 8/64 of the patients [16].
SPPH following caesarean section is not uncommon, but is
unlikely to be associated with retained placental tissue. However,
uterine artery pseudo-aneurysms (UAP) or arterio-venous mal-
formations (AVM) have been identied as potential cause of SPPH
following caesarean section [17,18]. It might not be easy to
distinguish between either of these conditions and uterine wound
angle necrosis (WAN) following caesarean section.
A lower uterine incision, made close to the relatively avascular
cervix, may predispose to WAN. So also is erosion of the uterine
artery, secondary to infection. The differences between UAP/AVM
and WAN are better appreciated by imaging techniques. A review
of recent obstetric-surgical notes might help. Clinical features of
UAP are not consistent. On many occasions, the diagnosis of WAN
is only made at exploratory laparotomy, at which debridement,
Suggested
Variant pattern of lochia rubra
Sub-involution of the placental implantation site
Abnormally adherent isolated lobe of placenta
Von Willebrands disease/Haemophilia A carrier/Factor XI deciency/Factor VII deciency/
Un-adjusted anticoagulant therapy
Post caesarean wound dehiscence
Endomyometritis
Vascular malformation of the uterus
Non-uterine bleeding
Pseudoaneurysm of the uterine artery
Gestational trophoblastic disease
 I.A. Babarinsa et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 159 (2011) 255260
repair or hysterectomy might be indicated. Uterine artery
embolisation has a complementary or denitive role in all three,
provided that there is an easily accessible interventional radiology
service, and the patients clinical status is stable [19].
Uterine artery pseudoaneurysm may result in a haematoma,
may rupture and exanguinate the patient as a revealed or
concealed bleed. It may follow pelvic surgery (including curettage),
gestational trophoblastic disease, inammation or normal vaginal
delivery [20].
Women with leukaemia and lymphoma patients may be at
an increased risk for SPPH [21]. SPPH is 1520 fold more likely
in women with von Willebrands disease [6]. Equal proportions
(11% each) of primary postpartum haemorrhage and SPPH,
occurred in 61 pregnancies in women with Factor XI deciency
managed over 10 years in a tertiary-care setting in London
[22].
Persistent SPPH in a 28 year old was eventually found to be due
to an endometrial stromal sarcoma [23]. Five of the 9 consecutive
women documented at Shefelds trophoblastic Diseases Centre
who had choriocarcinoma following term non-molar pregnancies,
had SPPH [24].
4.1. Investigations
SPPH attributable to retained placental tissue or membranes is
easily treatable, and should be excluded as soon as possible.
However, this is often not as simple as it would appear. The uterus
containing retained products may not initially bleed. Indeed, the
cervical os may be closed.
Ultrasound scans are commonly performed for SPPH, with the
specic aim of ruling out retained products of conception. This
should help exclude patients from an unnecessary surgical
procedure. Mulic-Lutvica and Axelsson [25] found that the nding
of an echogenic mass in the uterine cavity, combined with a cavity
diameter above the 90th centile was associated with retained
placental tissue. They caution however, that even though
ultrasound technology has become more powerful, demonstration
of retained tissue is still difcult.
A pelvic ultrasound scan performed for SPPH could be deemed an
incomplete investigation, if a colour ow Doppler study of the
placental bed was not concurrently undertaken. Suspicion of a
possible arterio-venous malformation or pseudoaneurysm of the
uterus (UAP) may be made from nding an anechoic or hypoechoic
pulsatile well dened para-uterine or uterine mass on pelvic scan.
Doppler conrms the presence of turbulent ow within the cystic
structure [26,27]. The use of pelvic ultrasound scan, colour Doppler
ultrasound, CT angiography and digital subtraction angiography
have achieved better sensitivity.
To the best of our knowledge, there is scant published evidence
to indicate that the ndings on a postpartum pelvic ultrasound
can specically guide the best option of treatment. Some workers
propose that uterine evacuation may be the appropriate
treatment for the nding of enhanced myometrial vascularity,
seen on Doppler imaging in combination with placental
remnants [28].
Islands of unsuspected morbidly adherent placenta may be
the reason for recurrent SPPH after conservative management,
or even after suction evacuation. This may be one rare indication
for hysteroscopy for SPPH. A repeat curettage was noted to be
less likely after a hysteroscopic selective curettage [29]. It was
observed that hysteroscopic resection of retained placental
tissue was not complicated by endometrial adhesions.
In practice, most women with coagulation disorders are known
antenatally and the Haematologists would normally have a
detailed management plan. It is therefore the rare patient with
persistent, recurrent or unexplained SPPH who might require a
257
baseline check of a Platelet count, Prothrombin Time and Activated
Partial Thromboplastin Time. Abnormalities of these should
warrant involvement of the Haematology service with a view to
factors assay(s). If a patient has been on therapeutic doses of
anticoagulants, this will obviously need to be reviewed.
4.2. Management
Most SPPH will settle without the patient requiring investigation or
any specic treatment.
It is difcult to reassure a patient that SPPH will eventually stop
without doing anything. The patient expects some intervention
and a course of antibiotics is likely to be appreciated by the
patient!
When a patient presents to a healthcare facility however, three
questions need to be answered:
i. is she unwell?
ii. is the bleeding heavy and on-going?
iii. is she merely worried that the bleed has persisted beyond her/
family expectations?
If the cause of the SPPH is known, then treatment should be
specic and focused on the possible underlying pathological
process.
The specic treatments for SPPH are conservative, pharmaco-
logical or surgical; or by interventional radiology. This depends on
the clinical ndings, the hospitals standard practice or protocols,
practitioner experience and the choice of the patient.
A personal, family and medication use history may be
useful in narrowing-down the possible causes of SPPH. After
endomyometrial causes have been excluded, it is also reason-
able to consider systemic causes of depletion or dysfunction of
platelets and/or clotting factors or other chronic medical
disorders in which SPPH may occur as a consequent or collateral
morbidity.
It is not out of place to warn the patient that the treatment of
SPPH is not as clear-cut, and major life-saving surgery may be
rarely indicated.
If a conservative approach is decided upon, agreed criteria
should be set for when a review should occur e.g., 5 days after
initial consultation. Any increase of loss; symptoms compatible
with anaemia or a dened drop in haemoglobin level, or ongoing
patient concerns, should prompt earlier review.
Choice of a pharmacological treatment should take into account
the secretion of the agent or its metabolite into breast milk [30], its
interaction with other drugs and the duration of treatment
required. Table 2 summarises selected published papers on the
medical management of SPPH.
We would suggest practical management strategies based on
rst principles:
 If the patient is not unwell, not anaemic, and not tachycardic and
SPPH is not heavy or increasing, it is reasonable to reassure and
observe for a few days and make arrangements for regular review,
or for her to keep in touch at agreed and dened intervals.
 If there are no demonstrable retained products on pelvic scan, no
abnormal ndings on uterine Dopplers, but the bleeding is
persistently heavier than patients own menstrual blood loss, a
course of oral Misoprostol [rst week post-partum] or Tranexa-
mic Acid [after the second week] could be considered. It is
important to inform the patient that such agents are not
specically licensed for this purpose [38].
 Any patient with SPPH who presents for the rst time (or in
whom SPPH persists) after 6 weeks, may benet from a course of
258 I.A. Babarinsa et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 159 (2011) 255260

Table 2
Medical management of secondary postpartum haemorrhage (from selected publications).

Agent(s) Dose/regime Comment Evidence level Reference

Misoprostol 800 mg, intra-uterine [stat] Immediately following uterine III [31]
evacuation in theatre
Antibiotics. . . Not stated 12 of 57 women required evacuation III [32]
after initial antibiotics
. . .Uterotonic agents and/or antibiotics. . . Oxytocin infusion; Methylergonovive IV [33]
0.2 mg [IM], and Q 24 h  3 doses;
haemabate 250 mg [IM] Q 15 min  8
doses if necessary
Tranexamic acid Not stated Specically for SPPH in women with [34]
bleeding disorders. Note that agent
is used for menorrhagia in women
without bleeding disorders!
Prostaglandin E2 suppositories 3 mg [intra-uterine] Post-curettage III [35]
. . .Antibiotics and uterotonic drugs Not stated Were ineffective the 14 women who III [36]
(IV). . .oxytocin or sulprostone had suspected retention endometritis
and angiographic cause of SPPH
before embolisation treatment
. . .Conventional treatment involves No additional benet from Specically addresses the regime Ib [37]
antibiotics and uterotonics. . . extended oral therapy for Postpartum endometritis
Ampicillin (or clindamycin) and
metronidazole with or
without gentamycin (IV)

Combined Oral Contraceptive pills or Norethisterone tablets,
provided that her serum b-hCG is zero.
Uterotonics have been listed amongst the options for treating
SPPH [39]. With antibiotics, they are thought to reduce the need for
curettage. However Jacobs [33] pointed out that uterotonics will
not be useful, if the uterus is rm.
The British National Formulary [40] states that: mild secondary
postpartum haemorrhage has been treated in domiciliary practice
with ergometrine by mouth, but it is rarely used now (page 399).
Oral or rectal Misoprostol would appear to be acceptable
alternatives for the management of SPPH given its safety prole in
managing primary post-partum haemorrhage. A dose of between
200 mcg and 1 mg (15 tablets) has been variously tried the only
common side effect being transient diarrhoea and abdominal
cramps.
Trans-cervical intra-uterine administration of 3 mg of Prosta-
glandin E2 has been used to successfully manage a patient who had
persistent vaginal bleeding following an 8th day SPPH for which
evacuation-curettage had been done [41].
Tranexamic acid is the rst line choice for managing many non-
traumatic PPH associated with von Willebrands disease [42]. It has
been used to prevent and control obstetric haemorrhage following
caesarean section and abruptio placenta with no reported neonatal
sequelae. Kominiarek and Kilpatrick [43] hypothesize that it is
possible that a coagulation disorder, inherited or acquired, is
responsible for many cases of PPH without a clear cause.
Tranexamic acid may therefore be one reasonable option in the
management of SPPH of uncertain aetiology [34].
In the proposed management owchart below (Fig. 1), we
suggest treatment with Misoprostol in the weeks proximate to
childbirth, since it is likely that the vascular dysfunction [12,13] is
relevant. Following the sixth postpartum week, some clinicians
manage any ongoing loss as a pseudo-dysfunctional uterine bleed
rather than as a specic SPPH. Antibiotics were prescribed in the
study by King et al. [16] for almost all the women.
Neill and Thornton [12] in an unpublished observation, noted
that nearly 10% of women with SPPH were prescribed Norethis-
terone, probably equating the pathophysiology with Dysfunctional
Uterine Bleeding. Whilst this may work after the 6th post partum
week, it is debatable if it will, before then.
Hitherto, curettage was regularly resorted to, for SPPH
management. Boyd et al. [1] managed 88% of their SPPH patients
with surgical curettage. They justied this by claiming that even
without retained products patients with probable abnormal
involution of the placental site do well with curettage. Such
instrumentation may not only disturb thrombi providing hae-
mostasis, but is also likely to disrupt the walls of any pseudo-
aneurysm [44]. In the study by Feigenberg et al. [45], hysterecto-
my, blood transfusion, perforation of the uterus and systemic
infection were more than twice as likely in women who had
surgical rather than medical management of SPPH. If surgical
intervention is planned, it is best that an experienced Obstetrician
undertakes it.
When profuse bleeding complicates uterine evacuation or
SPPH, senior help must be sought and resuscitative measures
commenced promptly. As the source of the bleeding is within the
uterus, contractility-enhancement, tamponade, and vascular
compression measures should be commenced. These may include
the use of endo-uterine balloons [46], compression sutures [47] or
hysterectomy, as measures of last resort.
A Canadian Group [27] have proposed an algorithm for the
management of SPPH. One of their suggestions is that pelvic
angiography +/ embolisation be considered when the diagnosis is
unclear from a pelvic ultrasound in a stable patient. With such a
policy, a signicant proportion of women will either have invasive
procedures with low yield or, arguably, negligible measurements.
We feel that our proposed owchart is compliant with
ambulatory care, operable by General Practitioners and Commu-
nity Midwives. Rather rigid time-scales have been set, to which
most concerned patients will agree: aiming to signicantly reduce
the volume of reported blood loss within the rst 72 h, and
achieving no more than spotting by the end of one week.
It clearly needs to be modied or adapted to local needs, and
audited from time to time.
5. Prediction and recurrence
The main predictive factor for SPPH is a past history of a similar
past experience [48]. The odds ratio for other risk factors included:
a primary postpartum haemorrhage in the index pregnancy {4.7},
and maternal smoking or vaginal bleeding before 24 weeks of
index pregnancy {3.0}.
 I.A. Babarinsa et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 159 (2011) 255260
Fig. 1. Suggested owchart in SPPH management. Abbreviations: ET, endometrial thickness measurement is from RCOG Green-Top guideline [No. 25], where below this
measure, retained products are unlikely to be conrmed histologically [53]; HCG, human chorionic gonadotrophin; MBL, menstrual blood loss; N, normal; SPPH, secondary
postpartum haemorrhage; TVUS, trans-vaginal ultrasound scan; TXN, Tranexamic; UAE, Uterine artery embolisation.
SPPH recurred in nearly 19% of 32 multiparae in a retrospective
review of women in two hospitals in the United Kingdom [49].
In a cross-sectional interview of 724 patients, some 26 weeks
after childbirth in the USA, 97% of women who had reported
vaginal bleeding felt inadequately prepared for it [50].
Physicians should also be prepared to employ the spectrum of
management options for SPPH, which may range from vasopressin
to clotting factor concentrates to selective arterial embolisation
[51].
The current patient information leaets about postpartum care
need to specically address the uncertainties about the causes and
treatment of unexplained SPPH.
6. Conclusion
Six years ago, a Cochrane Review found no randomised trials on
treatments for SPPH [52].
To the best of our knowledge, there are still none. Patients need
to be told this, and that our current treatment options, in the
absence of a clear cause of SPPH, are empirical.
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