Hum. Reprod.-2005-Farquharson-3008-11

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Human Reproduction Vol.20, No.11 pp.

30083011, 2005

doi:10.1093/humrep/dei167

Advance Access publication July 8, 2005.

Updated and revised nomenclature for description


of early pregnancy events
Roy G.Farquharson1,4, Eric Jauniaux2 and Niek Exalto3 on behalf of the ESHRE Special
Interest Group for Early Pregnancy (SIGEP)
1

Department of Obstetrics and Gynaecology, Liverpool Womens Hospital, Liverpool, Crown Street, Liverpool L8 7SS, 2Academic
Department of Obstetrics and Gynaecology, Royal Free and University College London Medical School, London, UK and 3Department
of Obstetrics and Gynaecology, Spaarne Ziekenhuis, Hoofddorp, The Netherlands
4

To whom correspondence should be addressed. E-mail: [email protected]

Key words: early pregnancy/nomenclature

Introduction: recognizing the changes


The commonest early pregnancy complication of spontaneous
miscarriage occurs in approximately 1520% of all pregnancies, as recorded by hospital episode statistics. The actual
figure, from community-based assessment, may be up to 30%,
as many cases remain unreported to hospital (Everett, 1997).
The great majority occurs early, before 12 weeks gestational
age and fewer than 5% occur after identification of fetal heart
activity (Brigham et al., 1999). Second trimester loss, between
12 and 24 weeks, occurs less frequently and constitutes <4% of
pregnancy outcomes (Ugwumadu et al., 2003). The clinical
assessment of every pregnancy loss history requires clarification of pregnancy loss type and accurate classification, whenever possible.
The traditional grouping of all pregnancy losses prior to
24 weeks as abortion may have had pragmatic origins, but it
is poor in terms of definition and makes little sense. The term
abortion is also confusing for the patient. She may not realize
that (spontaneous) abortion is not a termination of pregnancy
because medical abortion or legal abortion is used in the
same way.
Increasing knowledge about early pregnancy development,
with the more widespread availability of serum HCG measurement, the advent of high-resolution ultrasound and a clearer
description of gestational age at pregnancy loss make for a
more sophisticated assessment of miscarriage history but also
help the couples awareness from as early as 5 weeks of gestation.
The advent of these important information milestones has not

been fully realized or incorporated into clinical event description for article publication.
The emergence of early pregnancy units (EPUs) in many
hospitals has addressed the need for a dedicated clinical area
for the diagnosis of miscarriage and patient support at a distressing time (Twigg et al., 2002). With the establishment of an
EPU network, it becomes more important that a standardized
diagnostic classification system be employed for accurate and
reproducible reporting of ultrasound findings and clinical outcomes, so that direct comparisons between units can be readily
understandable for both research and audit purposes.
The most recent confidential enquiry into maternal deaths
conclusively demonstrates that mortality from ectopic pregnancy has not declined and is still increasing over and above
rates described 10 years ago (CEMACH Report, 2004). As the
EPU represents the most likely point of ectopic pregnancy
diagnosis, the importance of standardized reporting of very
early pregnancy changes requires a robust approach following
recent recommendations (Kirk et al., 2004).

Duration of pregnancy
Just as postnatal age begins at birth, prenatal age begins at
fertilization. The embryonic period occupies the first 8 postfertilization weeks, during which organogenesis takes place.
Thereafter, the fetal period is characterized by growth. Embryologists prefer the term embryonic age and assess this by
using 23 internationally recognized morphological stages

3008 The Author 2005. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology. All rights reserved.
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The nomenclature used to describe clinical events in early pregnancy has been criticized for lack of clarity and promoting confusion. There is no agreed glossary of terms or consensus regarding important gestational milestones. In
particular there are old and poorly descriptive terms such as missed abortion and blighted ovum, which have persisted since their introduction many years ago (Robinson, 1975) and have not undergone revision despite the widespread application of ultrasound for accurate clinical assessment and diagnosis. The authors are aware of these
shortcomings in terminology and are keen to provide an updated glossary. We hope that this paper will facilitate the
introduction of a revised terminology in an attempt to provide clarity and to enhance uptake and use in the literature
as well as clinical assessment and documentation.

Nomenclature for early pregnancy events

Ultrasound criteria
With the introduction of transvaginal ultrasound, longitudinal
assessment of early pregnancy development can be made in
terms of viability and growth. Ultrasound plays a major role in
maternal reassurance, where fetal cardiac activity is seen and is
pivotal in the assessment of early pregnancy complications,
such as vaginal bleeding (Jauniaux et al., 1999). However,
there are limits to ultrasound resolution of normal early pregnancy development. Recent advice concludes that a diagnosis
of an empty sac (previously named anembryonic pregnancy,
early embryonic demise or embryo loss) should not be
made if the visible crownrump length is less than 6 mm, as
only 65% of normal embryos will display cardiac activity
(Royal College of Radiologists/Royal College of Obstetricians
and Gynaecologists, 1995). Repeat transvaginal ultrasound
examination after at least a week, showing identical features
and/or the presence of fetal bradycardia, is strongly suggestive
of impending miscarriage (Chittacharoen et al., 2004). The
possibility of incorrect dates should always be remembered by
the alert clinician. In addition, it should be remembered that
when the fetus has clearly developed and the fetal heart is
absent, the term missed abortion should be replaced by
delayed miscarriage (Hutchon and Cooper, 1997).
Gynaecologists and ultrasonographers acknowledge the
embryonic period by speaking about fetal heart action and
fetal activity before the end of organogenesis. This evidence
is vital to the patient, who sees them as clear signs of life.
Embryologists, by contrast, may debate the meaning of
embryo in early pregnancy, but embryo is more synonymous

with cells in an IVF laboratory than as the preclinical scientific


description of anatomical organogenesis. Although a clear distinction between embryonic and fetal periods is significant in
teratology, we have to accept that modern terminology should
reflect daily clinical practice, in which description has changed
in the last two decades and is more patient-centred. The term
fetus receives an ultrasound definition that includes fetal
heart activity and/or a crownrump length >10 mm.
Classification of events
There has been a plea to classify pregnancy losses according to
the gestational age at which they occur and detail the event; for
example, in the case of fetal demise at 8 weeks, to define it as
fetal death at 8 weeks gestational age. In this way, possible
pathophysiological mechanisms may be postulated and studied. Historically, clinicians have grouped all pregnancy losses
that occur at a gestational age prior to theoretical viability
under the umbrella of abortion.
Between 1% and 2% of fertile women will experience recurring miscarriage (RM) (Stirrat, 1990). Recently, among
researchers in the field of RM, it has been recognized that the
classification of pregnancy loss is more complex as the developing pregnancy undergoes various important stages, and
different pathology at the time of pregnancy loss is exhibited at
these different stages. As the majority of RM cases following
investigation are classified as idiopathic (Stirrat, 1990), it is
generally accepted that within the idiopathic group there is
considerable heterogeneity and it is unlikely that one single
pathological mechanism can be attributed to their RM history.
Furthermore, there is considerable debate about cause and
association as the exact pathophysiological mechanisms have
not been elucidated. Current research is directed at theories
related to implantation, trophoblast invasion and placentation,
as well as factors which may be embryopathic.
The absence of an identifiable pregnancy on ultrasound
examination in combination with a positive urine or serum
HCG pregnancy test is named a pregnancy of unknown location
(PUL). Biochemical pregnancy loss is a better description
than trophoblast in regression or preclinical embryo loss. After
ultrasound identification of pregnancy, a miscarriage can be
classified as early (before 12 weeks) or late (after 12 weeks).
Heterotopic pregnancy is a combination of an intrauterine
pregnancy and an ectopic pregnancy. Hydatidiform mole
pregnancy and partial mole would be better replaced by
gestational trophoblastic disease, complete or partial.
Future direction
The revision of early pregnancy nomenclature is both desirable
and essential in raising the standard of reporting (Table I). To
improve the accuracy of observational studies, it is desirable to
present a clear and consistent description of the pregnancy
event that can be universally understood by the reader. For randomized controlled trials of treatments, it is essential to have a
clear classification of pregnancy loss type for both fetal and
very early loss events. In addition, there is a strong argument
for mandatory karyotyping of all pregnancy losses to exclude a
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(ORahilly and Muller, 2000). Clinicians, however, conventionally calculate from the first day of the last normal menstrual period (LMP). Confusion about the definition of
pregnancy duration derives from the use in the published literature of terms such as postovulatory age and conceptual age,
and even misnomers like menstrual age.
Clinicians do have to acknowledge that a woman does not
become pregnant during the LMP or during ovulation, but
exclusively after conception. Gestation is the condition of
being carried in the womb during the interval between conception and birth. The term gestational age (GA) is therefore
confusing, although generally accepted, and its widespread use
can only be legitimized by using a proper definition. The
appropriate way to overcome this confusion is to choose GA
based on a theoretical ovulation plus 2 weeks. As early ultrasound measurements of the fetus (crownrump length, CRL)
are reproducible (Pedersen, 1982) and more accurate than the
use of the LMP, there is a need in publications to define GA
based on LMP and/or ultrasound measurements.
The terms egg and ovum, sometimes used in clinical
publications, should be avoided because they have also been
used incorrectly for both an oocyte and an embryo (ORahilly,
1986). This author suggested that the term egg be reserved
for a nutritive object only. Similarly, the use of the term
embryo versus fetus is confusing as infertility specialists
use embryo in the preimplantation period while anatomists
use embryo until 8 weeks after implantation.

Roy G.Farquharson et al.

Table I. Glossary of terms and early pregnancy events


Avoid

Prefer

Ultrasound findings

Egg
Embryo

Oocyte
Fetus

Embryonic age
Postovulatory age
Conceptual age
Menstrual age
Threatened abortion
Spontaneous abortion
Medical abortion
Legal abortion
Recurrent abortion
Habitual abortion
Pregnancy test
Preclinical embryo loss

Gestational age based on last menstrual


period and/or ultrasound fetal measurement

Ultrasound-based definition to
include fetal heart activity and/or crownrump
length >10 mm

Threatened miscarriage
Spontaneous miscarriage
Termination of pregnancy

Fetal loss

Early abortion

Early pregnancy loss

Missed abortion
Late abortion

Delayed miscarriage
Late pregnancy loss

Hydatidiform mole
Partial mole
Molar pregnancy

Gestational trophoblastic disease


(complete or partial)
Heterotopic pregnancy
Pregnancy of unknown location (PUL)

No definition of pregnancy location


Pregnancy not located on scan
Gestation sac with absent structures or
minimal embryonic debris without heart rate activity
Previous identification of crownrump length
and fetal heart activity followed by loss of heart activity
Ultrasound definition of intrauterine pregnancy with
reproducible evidence of lost fetal heart activity and/or
failure of increased crownrump length over one week, or
persisting presence of empty sac, at less than 12 weeks gestation.
Same as for early pregnancy loss (see above)
After 12 weeks gestational age where fetal measurement
was followed by loss of fetal heart activity

Intrauterine plus ectopic pregnancy (e.g. tubal,


ceryical, ovarian, abdominal)
No identifiable pregnancy on ultrasound with positive
blood/urine HCG

Table II. Overview of commonest pregnancy loss events and ultrasound


Type of loss

Typical gestation
(range in weeks)

Fetal heart activity

Principal ultrasound finding

HCG level

Biochemical loss
Early pregnancy loss

<6 (06)
68 (410)

Never
Never

Low then fall


Initial rise then fall

Late pregnancy loss

>12 (1020)

Lost

Pregnancy not located on ultrasound


Empty sac or large sac with minimal
structures without fetal heart activity
Crownrump length and fetal heart activity
previously identified

lethal trisomy karyotype or triploidy. This is because, irrespective of treatment intervention, pregnancy loss has occurred and
may have been described as a false treatment failure. Recent
papers testify to the high rate of abnormal chromosome type
when pregnancy loss has occurred (Bricker and Farquharson,
2002; Levine et al., 2002; Stephenson et al., 2002; Philip et al.,
2003; Morikawa et al., 2004).
The authors understand that a modernized classification system
is not able to address every clinical scenario, but the adoption of a
revised terminology is a better way forward than persisting with
an antiquated description that precedes the universal use of transvaginal ultrasound findings or serum HCG levels, (Table II).
3010

Rise then static or fall

References
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Br J Obstet Gynaecol 104, 73.

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Trophoblast regression
Menstrual abortionpreclinical abortion
Early embryonic demise
Anembryonic pregnancy
Embryonic death

Recurrent miscarriage consisting of 3 early


consecutive losses or 2 late pregnancy losses
Serum/urine level of HCG
Biochemical pregnancy loss with description
of falling low positive serum/urinary HCG
Biochemical pregnancy loss
Biochemical pregnancy loss
Empty sac

Nomenclature for early pregnancy events


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Submitted on March 15, 2005; resubmitted on April 29, 2005; accepted on
May 4, 2005

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