Commentary

DOI: 10.1111/1471-0528.14071
www.bjog.org

Zika virus and pregnancy

D Lissauer,a,b E Smit,c MD Kilbya,b
a

Centre for Womens & Newborn Health, Institute of Metabolism and Systems Research, College of Medical & Dental Science, University of
Birmingham, Birmingham, UK b Fetal Medicine Centre, Birmingham Womens Foundation Trust (Birmingham Health Partners), Edgbaston,
Birmingham, UK c Public Health England, West Midlands Public Health Laboratory, Heart of England NHS Foundation Trust, Birmingham, UK
Correspondence: Professor MD Kilby, Academic Unit, Third Floor, Birmingham Womens Foundation Trust, Edgbaston, Birmingham, B15
2TG, UK. Email [email protected]
Accepted 13 March 2016. Published Online 6 May 2016.
Please cite this paper as: Lissauer DM, Smit E, Kilby MD. Zika virus and pregnancy. BJOG 2016;123:12581263.
Linked article: This article is commented on by RM Burke et al. on page 1264. To view this mini commentary visit http://dx.doi.org/
10.1111/1471-0528.14073. This article is part of a collection of articles on the Zika virus, introduced by an Editorial by SS Witkin, p. 1255
in this issue. To view this Editorial visit http://dx.doi.org/10.1111/1471-0528.14076.

Background
In early February 2016, the World Health Organization
(WHO) declared the pandemic outbreak of Zika virus
(ZIKV), predominantly in Central and South America, and
the potential association of this infection during pregnancy
with the development of microcephaly a public health
emergency of international concern. Dr Margaret Chan,
the WHO Director General, indicated that the association
of the viral illness and birth anomalies was an extraordinary event and a public health threat to other parts of the
world. Such a declaration will trigger a public health
response likely to mobilise international resources and
expertise. This follows similar concerns raised by the Centers for Disease Control & Prevention in the USA (CDC)
and Public Health England (PHE).

Transmission and clinical symptoms

Zika virus is a member of the virus family Flaviviridae,
genus Flavivirus, which includes other viruses such as West
Nile, dengue and yellow fever viruses with which the serological tests can cross-react. It is a 40-nm virus with icosahedral symmetry, and has a non-segmented, single-stranded,
positive sense RNA genome.1 It is transmitted by a vector,
the daytime active mosquitoes from the genus Aedes and of
multiple species, most commonly Aedes aegypti.2 It is
important to note that these mosquitoes are not present in
the UK. After a mosquito bites a human, the first symptoms
of ZIKV can develop within 312 days. The WHO case definition of a suspect is someone with a compatible travel history and rash or fever and one of conjunctivitis, arthritis or
arthralgia. Likewise, the Royal College of Obstetricians and
Gynaecologists (RCOG) testing algorithm suggests that

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clinical illness is consistent with two or more symptoms

from fever, maculopapular rash, arthralgia or conjunctivitis.
However, the majority of individuals have minimal symptoms or may be asymptomatic.1 Typically within 2 days the
rash fades, and within 3 days, the fever resolves and only
the rash remains for up to a week. ZIKV has been a relatively mild disease of limited scope but may be associated
with serious illness. Indeed, there have been reports of
increased prevalence of GuillainBarre syndrome3 in areas
affected by ZIKV outbreaks, and a recent study reported
ZIKV infection a median of 6 days before the onset of GuillainBarre syndrome in a large series of patients,4 providing
more evidence of a causal relationship.

Epidemiology
Dengue fever has been present in South America since at
least the 1880s and is commonly found worldwide.5
Chikungunya virus was first reported in the Central and
South American continent in September 2014.6 The dengue
and chikungunya outbreaks are associated with ZIKV, in
that they share the same transmission dynamics. Hence, the
same population and environmental factors drive the
spread of all three diseases and there is valid concern that
the ZIKV will become as widespread. However, the arrival
of ZIKV into South America is thought to be separate from
the arrival of Chikungunya disease.7 There is also molecular
evidence that spread of the pandemic ZIKV lineage is associated with a recent genetic adaptation in humans, which
could facilitate viral replication and increase viral titres.8
ZIKV was initially discovered in a Rhesus monkey in
Uganda in 1947 and then transmission was noted in
humans by the end of this decade.1 The first reported epidemic reported outside Africa and Asia occurred in

2016 Royal College of Obstetricians and Gynaecologists

Zika virus and pregnancy

Micronesia in 2007. Since then there have been further outbreaks, of the same strain, in French Polynesia (in 2013),
followed by further major outbreaks, starting in Easter
Island (February 2014) and currently spreading rapidly
across Central and South America. The current South
American ZIKV epidemic was first reported in May 2015.

Vertical transmission and possible

association with congenital
microcephaly
The main mode of human-to-human transmission is vector-borne, through the bite of infected mosquitoes. Pregnant women may be infected in any trimester9,10 with
transmission of ZIKV also documented throughout pregnancy. However, there is not yet any evidence for whether
any particular trimester of vertical infection leads to higher
rates of fetal mortality or morbidity. The CDC and the
WHO have also recently concluded that there is substantial
evidence that the ZIKV can be sexually transmitted.11
The incidence of ZIKV infection in pregnant women in
affected countries is not currently known, and data on
numbers of pregnant women infected are presently limited.
No evidence exists to suggest that pregnant women are
more susceptible to ZIKV infection or that the disease is
more severe during pregnancy.
Although ZIKV RNA has been detected in pathological
specimens of placenta and amniotic fluid from fetal losses,9
it is not known if this infection leads to increased rates of
pregnancy loss.
In October 2015, the Brazilian Ministry of Health
reported an unusual increase in the number of babies born
with microcephaly.12 By the end of last year, 1248 cases
(99.7 per 100 000 live births), including seven deaths, were
reported across Brazil (with a previous comparative rate of
5.7/100 000 livebirths in 2010); a 20-fold increase.
Previous ZIKV infection has been noted in women with
infants with microcephaly.9 It has been demonstrated that
ZIKV can cross the placental barrier and the virus has
been detected in blood and neurological tissues of at least
seven affected fetuses/infants; the mothers in six of these
cases presented with symptoms consistent with ZIKV
infection during pregnancy.13,14 The Ministry of Health in
Brazil has therefore suggested a possible relationship
between Zika infection and this unusual increase in babies
born with microcephaly. In addition, there have been
increasing numbers of reported central nervous system
malformations in fetuses and newborns in French Polynesia following an epidemic of ZIKV. In that case, only four
out of the 17 women who gave birth to children with central nervous system anomalies were tested for flaviruses.
All four women tested had positive serology (positive for
IgG, rather than IgM), which means that exposure to the

2016 Royal College of Obstetricians and Gynaecologists

virus could have been some considerable time previously.15 Concerns about the overdiagnosis of microcephaly
in all babies born to ZIKV-infected pregnant women is
valid, because of the use of an overly broad definition of
this condition, but the strength of this association is striking. Current ongoing studies are likely to provide definitive evidence of the relationship between ZIKV infection
in pregnancy and microcephaly and possibly other neurological defects in these babies. The WHO concluded with
a statement on the 28 January 2016 that a causal relationship between ZIKV infection, birth defects and neurological syndromes has not been established, but is strongly
suspected.
The gestation at which maternal ZIKV infection occurs
may be important. In one study, from Brazil, of 35 cases of
microcephaly in 26 (74%) women it was reported that they
had a rash during pregnancy. Of these, 21 occurred in the
first trimester, five in the second trimester and none in the
third trimester.16 Based on this information and on experience from other congenital infections such as cytomegalovirus, rubella virus and toxoplasmosis, it is likely that ZIKV
infection in early (first trimester) pregnancy poses the
greatest risk.
However, the risk needs to be put in context. In this
geographical region with the highest risk of ZIKV, the estimated absolute risk of an affected baby is 4 per 1000. This
means that even in the highest risk areas there is a 99.6%
chance of having an unaffected baby.

Management of the pregnant women

Objective knowledge about ZIKV and pregnancy is limited
and still evolving. Recommendations presently are based on
current information and are likely to be updated periodically
to reflect emerging evidence (Box 1). The current version of
the guidance should be used to inform patient care
(available at: https://www.gov.uk/government/publications/
zika-virus-interim-algorithm-for-assessing-pregnant-womenwith-a-history-of-travel).
In women who are pregnant or who are considering pregnancy, the advice from the CDC in the USA and PHE in the
UK is to postpone travelling to areas where the ZIKV
infection is ongoing for which there is a current ECDC
country checklist which should be consulted (available at:
ecdc.europa.eu/en/healthtopics/zika_virus_infection/pages/
index.aspx, accessed March 2016). If a pregnant woman
travels to an area with high rates of ZIKV transmission, she
should be advised to:
 avoid mosquito bites: by wearing long sleeves and trousers
 use registered insect repellents (insect repellents containing DEET, picaridin and IR3535 are safe in pregnancy)
including permethrin-treated clothing and

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Lissauer et al.

 sleep in screened (with mosquito nets) and air-conditioned rooms.

Women should be advised to avoid becoming pregnant
while travelling in an area with active ZIKV transmission.
On returning to the UK, they should avoid becoming pregnant for a further 28 days (based upon a 2-week incubation period and a further 2 weeks to clear the virus if
infected).
The risk of sexual transmission of ZIKV is thought to be
very low. The virus has been identified in the semen of
men who have had ZIKV infection but it is not known
how long this can persist. If a womans partner has travelled to a country with active ZIKV transmission, effective
contraception is advised to avoid pregnancy (and the use
of condoms should be considered to prevent against infection acquisition):
 for 28 days after his return home if he had no ZIKV
symptoms, either while abroad or within 2 weeks of his
leaving the affected country
 for 6 months following recovery if he did experience
ZIKV symptoms during that period
 women who have travelled to a ZIKV-affected area and
present with symptoms should also be seen and assessed by
a clinician (preferably one familiar with management of
returning travellers) to ensure that they are not unwell or
requiring other medical management.
Healthcare providers should ask all pregnant women
about recent travel and be mindful of the potential risk of
ZIKV.
Pregnant women with a history of travel to an area of
high risk and who present with symptoms (consistent with
ZIKV disease) during or within 2 weeks of travel, should
be tested for ZIKV infection and other travel-associated
infections (including malaria, dengue and chikungunya
virus infections). It is particularly important that other
more common causes of infectious skin rashes in pregnancy, including HIV and syphilis, are also excluded when
managing someone who is understandably extremely anxious about ZIKV infection. The need for assessment by a
physician familiar with management of infection in returning travellers must also be considered.
The only diagnostic service in the UK is provided by
the Rare and Imported Pathogens Laboratory (RIPL).
Patients are typically viraemic in the first 7 days of infection and ZIKV-specific polymerase chain reactions
(PCRs) can be used to identify these patients during this
period. Viraemia decreases over time, so a negative blood
PCR collected 57 days after symptom onset does not
exclude infection and one would therefore have to rely
on further serology to exclude recent infection.16 There
is some evidence that the viraemia can last longer in
urine, which will increase the sensitivity when screening
symptomatic patients.17

1260

Diagnostic testing is therefore currently only indicated in

those who are within 2 weeks of return to the UK with
active symptoms at time of assessment. Unfortunately there
is currently a lack of validated specific serological assays
(ZIKV IgM and IgG) in the UK. Serological assays also suffer from cross reactivity to other Flaviviruses but specificity
can be increased by confirmatory neutralising antibody
testing. It would be most useful to use serology to screen
asymptomatic patients who may have been infected to
guide clinical follow up when these tests become available.
The CDC has recently changed their recommendation for
asymptomatic travellers and now recommends that there is
no need for serial ultrasounds if the ZIKV IgM test result
is negative 212 weeks after travel. RIPL is currently validating different serological tests, but it is anticipated that
this service will not be available in the UK for some time.
It is therefore important to manage the expectations of
pregnant women who have recovered from their symptoms
or those who are afraid that they may have had an asymptomatic infection and not give them the impression that
there is a test that can exclude infection. The emphasis at
this stage should therefore not be on diagnosing the
infected mother but rather on an effective ultrasound
screening programme, which should be able to diagnose an
affected fetus.
The maternal samples required are a clotted blood (or
serum) and an EDTA blood (or plasma) sample along with
a small volume of urine (without preservative). The samples must be submitted with the RIPL request form (available on line from PHE). Given the overlap of symptoms
and endemic areas with other viral and bacterial infections,
RIPL will routinely test symptomatic pregnant women
returning from ZIKV-affected areas for other infections as
well as ZIKV. For asymptomatic women, RCOG recommends keeping a serum sample locally should future serological tests become available.
Where ZIKV is identified (or is inconclusive) on laboratory PCR testing, the pregnant woman should be referred
to a fetal medicine service for further assessment. If the test
for ZIKV is negative, serial (4-weekly) fetal ultrasound
scans should be considered to monitor fetal growth and
anatomy. Testing for ZIKV is not recommended for
women whose symptoms have resolved by the time of presentation, but they too should be offered serial (4-weekly)
fetal ultrasound scans. Routine testing of asymptomatic
women (those who remained asymptomatic while travelling
and for 2 weeks after their return from a ZIKV-affected
area) is not recommended. However, serial fetal ultrasound
scans as above should be considered (because ZIKV infection is associated with minimal symptoms in most people)
(Figure 1).
Any woman in whom microcephaly is suspected in her
fetus (fetal head circumference >2 SD below the mean for

2016 Royal College of Obstetricians and Gynaecologists

Zika virus and pregnancy

Pregnant woman with history of

travel during pregnancy to an area
with active ZIKV transmission in
the last 9 months3
Pregnant woman reports
clinical illness consistent
with ZIKV disease during
or within two weeks of
travel4

Pregnant woman does NOT

report clinical illness
consistent with ZIKV disease
during or within two weeks of
travel4

Currently symptomatic

Symptoms resolved

Submit serum, EDTA

plasma and urine
samples for testing at
RIPL5

Negative ZIKV PCR

result(s)6

Positive (or inconclusive)

ZIKV PCR result(s)

Baseline fetal ultrasound

and refer to fetal
medicine service for
further evaluation and
follow up8

Offer baseline fetal

ultrasound7. (If ultrasound
normal, consider repeating
every four weeks through
pregnancy)

If abnormal ultrasound
findings (eg small head9 or
intracranial calcifications10) or
additional concerns, refer to
fetal medicine service

Figure 1. Interim algorithm1 for assessing pregnant women with a history of travel during pregnancy to areas with active ZIKV transmission2 (PHE).
1
Interim guidance will be updated as more information becomes available. Currently this algorithm applies to women at all stages of pregnancy
although based on information available from Brazil and experience from other congenital infections (such as cytomegalovirus, rubella and
toxoplasmosis), infection in early pregnancy is likely to be the greatest risk.2 Laboratory testing is performed by the PHE RIPL. Given the overlap of
symptoms and endemic areas with other viral and bacterial infections, RIPL will routinely test symptomatic pregnant women returning from areas
with active ZIKV transmission for dengue virus, chikungunya virus and other infections as well as ZIKV. ZIKV testing will be performed exclusively
using real-time PCR rather than any serology test.3 Areas of active ZIKV transmission are countries and territories reporting active ZIKV transmission in
the last 9 months [http://ecdc.europa.eu/en/healthtopics/zika_virus_infection/zika-outbreak/Pages/Zika-countries-with-transmission.aspx].4 Clinical
illness is suggestive of ZIKV disease if two or more of the following symptoms are present at the time of assessment: fever; rash; arthralgia/arthritis;
conjunctivitis; myalgia; headache; retro-orbital pain; pruritus. Testing can also be considered for symptomatic pregnant women with acute onset of
symptoms within 2 weeks of travel to an area with active ZIKV transmission if the symptoms are not explained by other common infectious causes
(e.g. upper respiratory tract infection, urinary tract infection).5 The samples required are a clotted blood (or serum) sample, an EDTA purple top
blood (or plasma) and a small volume of urine without preservative. The samples must be submitted with a single RIPL request form (https://
www.gov.uk/government/publications/rare-and-imported-pathogens-testing-form-to-submit-sample). The form must clearly state the pregnancy
gestation and both the travel history (i.e. which countries visited and the dates of the outward and return journeys) and the clinical details (i.e. the
patients symptoms and the date of illness onset). This is so that the appropriate investigations can be performed and their results can be correctly
interpreted.6 If an alternative diagnosis is made there is no need for further ZIKV-specific laboratory follow up.7 For women without current
symptoms, taking and storing a clotted serum sample locally, without immediate testing, is recommended. In the event that there is a later concern
about fetal development, this sample will be available for retrospective testing, including detection of Zika antibodies, if an appropriate serological
test is available.8 This evaluation and follow up are likely to include repeat fetal ultrasound at 4-weekly intervals, and consideration of fetal magnetic
resonance imaging. Abnormal fetal findings will prompt appropriate investigation including, for example, submission of booking and current serum
samples for Toxoplasma, rubella virus, parvovirus and cytomegalovirus serology. Amniocentesis may be considered for ZIKV PCR.9 In this context,
small fetal head is defined as: head circumference >2 SD below the mean for gestational age, i.e. below the 2.5th centile.10 Apart from
microcephaly and intracranial calcifications, other brain abnormalities that have been reported in association with ZIKV infection are ventriculomegaly,
cell migration abnormalities (e.g. lissencephaly, pachygyria), arthyrogryposis (congenital contractures) secondary to central or peripheral nervous
system involvement.

gestational age [<2.5th centile]) or with a fetal brain

abnormality (such as intracranial calcifications or ventriculomegaly) diagnosed on ultrasound, and who has previously visited a ZIKV-affected area during pregnancy,

2016 Royal College of Obstetricians and Gynaecologists

should also be referred to a fetal medicine service for further assessment.

The majority of pregnancies screened and considered to
have a fetus with a head circumference > 2 SD below the

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Lissauer et al.

mean will be normal and will not have microcephaly. However, the RCOG has recommended referral to a specialist fetal
medicine service (Figure 1).18 Microcephaly is usually diagnosed when a babys head circumference is even smaller than
this, or when the velocity of growth is poor, and usually when
associated structural abnormalities of the brain are suspected.
In such circumstances serial ultrasonography is required
along with specialist in utero magnetic resonance imaging.
The latter may diagnose small brain volumes, associated neuronal migration disorders and intracranial calcification (Prof
PD Griffiths, University of Sheffield, pers. comm.).
If fetal microcephaly or brain abnormality is diagnosed,
consideration should be given to performing an amniocentesis to test for the ZIKV RNA using PCR (ref. 14 and
ecdc.europa.eu/en/healthtopics/zika_virus_infection/pages/ind
ex.aspx). However, this decision should be taken only after
careful counselling. Amniocentesis is associated with a
small risk of miscarriage or preterm birth and should not
be performed before 15 weeks of gestation.19 The sensitivity
of molecular detection of ZIKV is not known and it may
be that, as with other fetal viral infections (i.e. cytomegalovirus), a recommendation is made that an amniocentesis is
only considered after 18 weeks of gestation (when the fetal
kidneys are producing sufficient urine) or > 6 weeks after
infection.20 Even if positive, it is not known how sensitive
or specific this test is for congenital infection, nor the likelihood of an infected fetus being overtly affected. Nevertheless, if there is fetal abnormality on ultrasound and ZIKV
PCR on amniocentesis is positive, then this makes it more
likely that the abnormality is ZIKV-associated and that the
outcome may have a poor prognosis. When a significant
brain abnormality or microcephaly is confirmed in the
presence of ZIKV infection, the option of termination of
pregnancy should be discussed with the woman, regardless
of gestation (as would be the case if ZIKV infection was
not suspected).21
This is a rapidly developing field of investigation. International research efforts are focused upon the better understanding of the biology of ZIKV and the pathogenesis of
disease secondary to maternal infection. This will hopefully
lead to improved diagnostic testing and treatments. Key to
this is the development of a vaccine. Due to relatively
scanty epidemiological documentation and data gaps surrounding our knowledge of ZIKV many organisations have
committed to ensuring the open and rapid sharing of data
unfolding during this international health emergency.

Conclusion
It appears that there is a pandemic outbreak of ZIKV particularly within the geographical region of Central and
South America. There is growing evidence that ZIKV infection in pregnancy may be associated with an excess risk of

1262

central nervous system anomalies, including microcephaly.

This is a rapidly developing public health situation and
more objective data are likely to aid management of this
disease and its effects upon pregnancy in due course. More
detailed epidemiological data linking these events are
needed and in the meantime a systematic approach to the
investigation and management of pregnant women and
their unborn babies is required.
Box 1. Sources of current information on Zika virus
Our understanding of the biology of Zika virus and its management is
rapidly changing. For up to date information we recommend the
following online resources:
 Clinical advice on Zika: assessing pregnant women following travel;
symptoms, transmission (includes sexual transmission), epidemiology
Public Health England
https://www.gov.uk/guidance/zika-virus
 World Health Organization; collected resources on Zika, including
situation reports
http://www.who.int/emergencies/zika-virus/en/
 Centers for Disease Control and Prevention; Zika virus resources
and information
http://www.cdc.gov/zika/

Disclosure of interests
None declared. Completed disclosure of interests form
available to view online as supporting information.

Contribution to authorship
DL, ES and MK edited and approved the manuscript.

Details of ethics approval

No ethical approvals required.

Funding
DL is funded by an Academy of Medical Sciences clinical lecturer starter grant which is supported by a collaboration of
The Wellcome Trust, Medical Research Council, British
Heart Foundation, Arthritis Research UK, Prostate Cancer
UK and the Royal College of Physicians. The ICMJE disclosure forms are available as online supporting information. &

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