Human Reproduction Vol.20, No.10 pp. 2893–2898, 2005
doi:10.1093/humrep/dei159
Advance Access publication July 8, 2005.
Revisiting the ovarian volume as a diagnostic criterion
for polycystic ovaries
Sophie Jonard1, Yann Robert2 and Didier Dewailly1,3
1
Department of Endocrine Gynaecology and Reproductive Medicine, and 2Department of Radiology, Hôpital Jeanne de Flandre,
CHRU, 59037 Lille, France
3
To whom correspondence should be addressed. E-mail: [email protected]
BACKGROUND: This study revisited the ovarian volume (OV) as a diagnostic criterion for polycystic ovaries
(PCO). Indeed, a threshold of 10 cm3 for the OV, chosen at the polycystic ovary syndrome (PCOS) international
consensus held at Rotterdam in 2003, was to date not based on appropriate studies such as receiver operator characteristic (ROC) curve analysis. METHODS: This prospective study included 154 women with PCOS, selected by using
the former National Institutes of Health criteria, who were compared with 57 women with normal ovarian function.
Ultrasound examination was performed between cycle days 2 and 7 with a 7 MHz transvaginal transducer.
RESULTS: Mean OV, ovarian area (OA) and follicle number (FN) values were significantly higher in the PCOS
group than in controls. The area under the ROC curve (AUC) was >0.9 for all three criteria, indicating a satisfactory
diagnostic potency for each. Concerning the OV, setting the threshold at 7 cm3 offered the best compromise between
specificity (91.2%) and sensitivity (67.5%). In comparison, specificity and sensitivity were 98.2 and 45%, respectively,
with a threshold at 10 cm3. Nevertheless, the highest AUC was obtained for FN (0.956) and then for OA (0.941).
CONCLUSIONS: OV is a good diagnostic criterion for PCO but, on the basis of the present data, we propose to
lower its threshold to 7 cm3. The FN >12 still appears as the best diagnostic criterion. The OA could be used as a
surrogate for OV in difficult situations.
Key words: follicle number/ovarian area/ovarian volume/polycystic ovaries
Introduction
Since the polycystic ovary syndrome (PCOS) international
consensus held at Rotterdam in 2003, ultrasound criteria are
now included in the definition of this disease (Balen et al.,
2003; Rotterdam ESHRE/ASRM-sponsored PCOS consensus
workshop group, 2004). These criteria include the ovarian
volume (OV) and the follicle number (FN), which have been
considered the key features of polycystic ovaries (PCO) for
>15 years (Adams et al., 1985). They are combined according
to the following definition: ‘either 12 or more follicles measuring
2–9 mm in diameter or increased ovarian volume (>10 cm3)’.
This choice was based on a literature review and on a discussion between experts.
However, data from the literature that were available at the
time of the consensus conference were stringent to various
degrees. Only appropriate procedures such as the receiver
operator characteristic (ROC) curve analysis (Zweig and
Campbell, 1993) allow setting the cut-off value of a given
parameter in order to obtain the best compromise between
specificity and sensitivity. At the time of the Rotterdam conference, such analysis was available for the FN exclusively, in
only one study performed by ourselves (Jonard et al., 2003).
This study showed that a threshold set at 12 follicles per ovary
offered the best compromise between sensitivity (75%) and
specificity (98%) to distinguish PCO from normal ovaries.
On the other hand, the choice of the threshold of 10 cm3 for
the OV was more empirical. It was based on the synthesis of
results from many studies in which the upper normal threshold
was simply defined as being either the maximal value of
controls or the 95th percentile of the control range (see Table I).
Although this guarantees a specificity near to 100%, it does not
necessarily offer the best sensitivity. These studies have
reported a mean OV >10 cm3 for normal ovaries, but some
found higher values (Adams et al., 1985; Fulghesu et al., 2001;
see Table I). Furthermore, in studies reporting on large-scale
ultrasonography in general populations of premenopausal
women, the highest normal OV values span up to 18 (Van
Nagell et al., 1990) or even 20 cm3 (Pavlik et al., 2000).
However, in some studies, the upper limit was defined as the
mean + 2SD, without logarithmic transformation of data
(Pavlik et al., 2000; Fulghesu et al., 2001). This yields an overestimation when the parameter is not normally distributed, as is
the case for the OV. Therefore, beside the issue of diagnosing
PCO, the upper normal limit of the OV still suffers from some
variability in the literature.
To clarify these issues, we decided to revisit the OV as a
criterion for PCO. To do so, we prospectively collected ovarian
© 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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2893
S.Jonard, Y.Robert and D.Dewailly
Table I. Results of some ultrasound studies described in the literature concerning the ovarian volume
Reference
Ultrasound examination
route
Volume threshold Percentage of patients
indicative of PCOS with clinical PCOS having
the volume criterion
Percentage of controls No. of studied
having the volume
patients
criterion
No. of studied
controls
Adams et al. (1985)
Yeh et al. (1987)
Pache et al. (1992)
Van Santbrink et al. (1997)
Atiomo et al. (2000)
Fulghesu et al. (2001)
TA
TA
TV
TV
TV
TV
>15 cm3
>10 cm3
>8 cm3
>10.7 cm3
>9 cm3
>13.2 cm3
0
0
0
0
˜45
5
17
25
29
48
40
30
33
70
˜70
41
˜70
21
76
108
52
330
32
53
TA = transabdominal; TV = transvaginal.
measures in a new series of patients and controls who were
selected without using ultasonographic criteria. We applied the
ROC procedure to the data in order: (i) to check whether 10 cm3
is the best threshold for OV; and (ii) to challenge the diagnostic
potency of OV against that of FN and of ovarian area (OA), OA
being the criterion that we used instead of OV to define PCO
in all our previous studies, prior to the Rotterdam consensus
(Jonard et al., 2005).
Materials and methods
Patient and control populations
This study was approved by the Institutional Review Board of
the Lille University Hospital. Informed consent was obtained
from all patients and controls before their inclusion in the
study.
Controls.
The control population consisted of 57 women with normal
ovarian function. These women were referred to our Department for IVF because of tubal and/or male infertility. Exclusion criteria included a history of menstrual disturbances (i.e.
cycle length either <25 days or >35 days), hirsutism [as
assessed by the modified Ferriman and Gallway (F–G) score >6],
serum level of prolactin >20 mg/ml, serum testosterone higher
than our previously reported upper normal threshold, i.e. 0.5 ng/ml
(Pigny et al., 1997), and hormonal treatment during the 3 months
prior to the study.
Patients with PCOS.
From 154 patients consecutively recruited by our Department
and defined as having PCOS according to the Rotterdam criteria (Rotterdam ESHRE/ASRM-sponsored PCOS consensus
workshop group, 2004), 98 were selected by using the National
Institutes of Health (NIH) criteria (Zawadski and Dunaif,
1992), i.e. association of an oligo-anovulation (our definition
of oligo-anovulation differs slightly from the NIH definition,
i.e. oligomenorrhoea or amenorrhoea or cycle length either <25
days or >35 days and/or ovulatory disturbances as assessed by
basal body temperature chart and/or serum progesterone level
<3 ng/ml in the luteal phase at day 24 in the cycle), and clinical
and/or biochemical signs of hyperandrogenism (F–G score >6
and/or testosterone level >0.5 ng/ml). The diagnosis of PCOS
was retained after exclusion of other aetiologies (congenital
2894
adrenal hyperplasia, androgen-secreting tumour or Cushing’s
syndrome). We used this former definition of PCOS in order not
to use the OV, OA or FN as selection criteria, since our goal was
to study their diagnostic potency, free from any inclusion bias.
Serum sampling
Blood sampling was performed during the early follicular
phase (i.e. between days 2 and 7 after the last menstrual period)
in both PCOS patients and control women, as described previously (Pigny et al., 1997). In PCOS patients, the last menstrual
period was either spontaneous or induced by the administration
of didrogesterone (10 mg/day during 7 days).
Pelvic ultrasound examination
We carefully applied the guidelines recommended by the
Rotterdam consensus conference (Rotterdam ESHRE/
ASRM-sponsored PCOS consensus workshop group, 2004).
Ultrasound examination was performed between cycle days
2 and 7 with a 7 MHz transvaginal transducer (Logic 400
General Electric, Milwaukee, USA). Ultrasound measurements were taken in real time, according to a standardized
protocol. The highest possible magnification was used to
examine the ovaries. After the longest medial axis of the
ovary was determined, the length and thickness were measured and the OA was calculated using a manual or automatic
ellipse to outline the ovary as described previously
(Dewailly et al., 2002). The OV was estimated after the
measurement of the length, width and the thickness and use
of the classical formula for a prolate ellipsoid: L × W × T × 0.523
(Sample et al., 1977; Adams et al., 1985; Orsini et al., 1985).
The FN was established as described previously (Jonard et al.,
2003) by scanning each ovary from the inner margin to the
outer margin in longitudinal cross-section. All follicles of
<9 mm, but >2 mm, were counted. Follicle diameter was the
mean of two recorded diameters in the longitudinal and
antero-posterior planes.
Patients in whom transvaginal ultrasonography was inappropriate (virgins or patients who refused) were excluded from the
analysis, as well as those in whom no follicle was seen in either
the right or the left ovary and/or in whom the ovarian area was
below the lower normal limit, i.e. 2.5 cm2. Patients with at least
one follicle >9 mm in diameter at ultrasonography, or a serum
estradiol level >80 pg/ml, were also excluded from the study so
as not to confound the data with the presence of a dominant
follicle or a corpus luteum.
Ovarian volume and polycystic ovaries
Statistical methods
25
For the OA, OV and the FN, the data used for statistical
analysis were the mean of recorded values for the left and right
ovaries. Statistical significance between mean values was
attributed to two-tailed P < 0.05.
ROC curves (Zweig and Campbell, 1993) were constructed to examine the diagnostic test performance, i.e. the
ability to discriminate between controls and patients with
PCOS. Sensitivity against (1 – specificity) was plotted at
each level, and the area under the curve (AUC) was
computed by the non-parametric Wilcoxon statistical test
(Zweig and Campbell, 1993). The AUC represents the probability of correctly identifying controls and patients with
PCOS. A value of 0.5 means that the test result is no better
than chance.
The statistical analysis was performed using Statview 4.5
(Abacus Concepts Inc., Berkeley, CA) and SPSS 11.5 (SPSS
Inc., Chicago, IL) for the ROC analysis.
Results
PCO
22,5
A
CONTROLS
20
17,5
15
12,5
10
7,5
5
2,5
0
Mean Ov Area (cm2)
Mean Ov Vol (mL)
60
Table II shows the main clinical, hormonal and ultrasound
features of patients and controls. Analysis of variance indicated no significant effect of the day of sampling and ultrasound examination (from 2 to 7 days after the last
menstrual) on the OA, OV or FN values (P = 0.97, P = 0.86
and P = 0.82, respectively). Mean OA, OV and FN values
were significantly higher in the PCOS group than in
controls (Table II).
Figure 1A and B shows that the 10th–90th percentile ranges
of OA, OV and FN for women with PCOS overlapped those of
controls. The highest individual values in controls were 5.7 cm2,
10.3 cm3 and 14, respectively.
PCO
CONTROLS
B
50
40
30
20
Diagnostic potency of OV
The AUC curve for OV (see Materials and methods) was
0.905 (Figure 2), indicating that the tested variable had a
satisfactory diagnostic potency. The ROC analysis also
allowed estimation of the sensitivity and specificity for a
given threshold (Table 3). A threshold at 10 cm3 offered a
good specificity (98.2%) but a weak sensitivity (45%). Setting
the threshold at 7 cm3 offered the best compromise between
specificity (91.2%) and sensitivity (67.5%) (Table III).
Table II. Main clinical and hormonal features in controls and in patients
with PCOS
Age (years)
Body mass index
(kg/m2)
Testosterone
(ng/ml)
Mean OA (cm2)
Mean OV (cm3)
2–9 mm FN
PCOS (n = 98)
Controls (n = 57)
Pa
27.2 (19.5–33.0)
27.9(20.1–40.8)
29.0 (24.5–35.0)
22.9 (19.0–31.5)
NS
<0.002
0.63 (0.37–0.94)
0.27 (0.13–0.42)
<0.0001
6.25 (4.50–8.65)
9.48 (5.69–16.78)
16.75 (10.0–30.0)
3.90 (2.90–4.80)
4.75 (3.11–6.86)
6.5 (4.5–10.5)
<0.0001
<0.0001
<0.0001
Values are expressed as medians with 10–90th percentile range in parentheses.
a
P level by Student t test; NS = non-significant.
10
0
2-9mm FN
Figure 1. Box-and-whisker plots showing the values of (A) OA and
OV, and (B) FN. Whiskers represent the 10–90th percentile ranges,
and the boxes indicate the 25–75th percentile ranges. The horizontal
line in each box corresponds to the median.
Diagnosis potency of FN
The AUC curve for the FN (0.956) (Figure 2) indicated a better
diagnostic performance than for the OV. The present data on
this new series confirm that a threshold set at 12 for the FN
offers the best compromise between specificity (97%) and
sensitivity (79%) (Table III).
Diagnosis potency of OA
The AUC curve for the OA yielded an intermediate value
(0.941) (Figure 2), between those for OV and FN. The best
compromise between specificity (77.6%) and sensitivity
(94.7%) was obtained with a threshold set at 5.0 cm2 (Table III).
2895
S.Jonard, Y.Robert and D.Dewailly
ROC curve for OV
Table III. ROC curve data
1,00
Area under
the ROC curve
Threshold
Sensitivity
Specificity
OA (cm2)
0.941
OV (cm3)
0.905
2–9 mm FN
0.956
4
4.5
5.0
5.5
6
6
7
8
9
10
10
11
12
13
14
15
95.9%
90%
77.6%
67%
53.1%
89.8%
67.5%
63.3%
53.1%
45.9%
91.5%
89.4%
79%
76.3%
68.9%
65%
55.4%
75%
94.7%
100%
100%
77.2%
91.2%
94.7%
98.2%
98.2%
85%
90.2%
97%
100%
100%
100%
Sensi tivity
,75
,50
,25
0,00
0,00
,25
,50
,75
1,00
1 - Specificity
ROC curve for OA
1,00
Sensi tivity
,75
,50
,25
0,00
0,00
,25
,50
,75
1,00
1 - Specificity
ROC curve for FN
1,00
Sensi tivity
,75
,50
,25
0,00
0,00
,25
,50
,75
1,00
1 - Specificity
Figure 2. ROC curves for OV, OA and FN.
Discussion
In this study based on a new series of controls and patients with
PCOS, we confirm that an increased OV is a reliable ultrasound criterion for the diagnosis of PCOS, as proposed by the
Rotterdam consensus conference (Rotterdam ESHRE/ASRMsponsored PCOS consensus workshop group, 2004). However,
our results indicated that the 10 cm3 threshold proposed by this
conference yielded an almost 100% specificity but a sensitivity
<50%. This was expected since this cut-off value was far
above the 90th percentile of our control range. We obtained
better results when the threshold was lowered to 7 cm3, but it
must be stressed that gaining an acceptable sensitivity for this
parameter (i.e. close to >70%) brings it close to unacceptable
specificity (i.e. close to <90%).
2896
The upper normal threshold proposed here for OV is much
lower than reported by some authors (Adams et al., 1985;
Yeh et al., 1987; Van Santbrink et al., 1997; Atiomo et al.,
2000; Fulghesu et al., 2001; see Table I) but it agrees with
others (Pache et al., 1992). Indeed, there is still a lot of
controversy in the literature about the normal upper limit of
OV, which varies from 8 to 15 cm 3, and even more (Adams
et al., 1985; Yeh et al., 1987; Pache et al., 1992; Van
Santbrink et al., 1997; Atiomo et al., 2000; Fulghesu et al.,
2001; see Table I). The main reason for this appears to be the
lack of standardization of the ultrasound procedure. In many
studies, OV was measured at random during the menstrual
cycle (van Nagell et al., 1990; DiSantis et al.,1993; Atiomo
et al., 2000; Pavlik et al., 2000). The mean OV can therefore
have been overestimated in some patients because of the
presence of growing follicles >10 mm or a corpus luteum
(Granberg et al., 1990). Indeed, Christensen et al. (1997)
showed by ultrasonography that OV changes during the
normal menstrual cycle, with the lowest values in the early
follicular phase and the highest values in the luteal phase.
When data were restricted to the very early follicular phase of
natural cycles, mean normal OV was only 4.5 cm3. Therefore,
setting the normal upper limit for OV requires strict adhesion
to the Rotterdam consensus conference guidelines (Rotterdam
ESHRE/ASRM-sponsored PCOS consensus workshop group,
2004), which recommend scanning cycling women in the
early follicular phase for the correct measure of OV and FN.
Also, OV diminishes with age from 25 years onwards (Pavlik
et al., 2000). Consequently, any study reporting on OV
should use a control group that is age-matched to the patient
population. Lastly, in some studies, the control group may
have included non-symptomatic patients with PCO, and this
may have skewed the distribution of OV to excessive highest
values (Christensen et al., 1997).
The substantial intra- and inter-observer variability observed
with OV measurement (Balen et al.,2003) is another reason
explaining the large differences between the upper limits of the
normal OV from one study to the other. This is due to the technical difficulty of obtaining strictly longitudinal ovarian cuts,
Ovarian volume and polycystic ovaries
which is an absolute condition for accurate measures of the
ovarian axis in each of the three planes (length, width and
thickness). This is particularly true in cases of non-ellipsoid
ovaries, and it must be recognized that any assimilation of OV
to a sphere or prolate ellipse is, at best, an estimate because of
the irregular shape of the ovary. This explains why OA yielded
better results than OV in the present study. Indeed, measuring
the OA is less operator dependent, providing the examination
is performed on a strictly longitudinal plane and outlining of
the ovary is done by hand with automatic calculation of the
outlined area. This last technique must be preferred to fitting
an ellipse to the ovary when the area is given by the machine,
since PCO are frequently non-ellipsoid (Jonard et al., 2005). In
support of the good reproducibility of OA measurement, we
found exactly the same figure as the one that we reported 10
years ago with an OA threshold empirically set at 5.5 cm2, i.e.
100% specificity and 66% sensitivity (Robert et al., 1995).
However, this threshold was a little too high as indicated by the
ROC data in the present study where the optimal cut-off value
for OA was 5.0 cm2.
It must be stressed that in all studies, including the
present one, the thresholds for ultrasound measures have
been established by comparing normal women with patients
with PCOS. All have omitted the difficult issue of multifollicular ovaries (MFO), as did also the Rotterdam consensus conference. Actually, there is no consensual definition
for MFO, although they have been described as ovaries in
which there are multiple (≥6) follicles, usually 4–10 mm in
diameter, with normal stromal echogenicity and, for some
authors, slightly increased ovarian sizes (Adams et al.,
1985). Since no histological data about MFO are available,
it is not known whether all stages of follicular growth are
involved and, hence, whether or not they represent an entity
distinct from PCO. Clinically, MFO are characteristically seen
in situations other than PCOS, mainly during normal puberty
and in women suffering from hypothalamic amenorrhoea
(HA). Although the clinical picture of HA is theoretically
different, the combination of amenorrhoea and PCO-like
features could erroneously lead to the diagnosis of PCOS if
one applied the Rotterdam definition too inflexibly. Such
an overlap between PCO and MFO emphasizes the need for
a careful exclusion diagnosis before applying the Rotterdam
criteria as well as for considering ultrasound criteria other
than FN and OV in difficult situations. This point raises the
question as to whether the OA should be preferred to OV.
Besides providing an accurate estimation of ovarian size,
freezing a longitudinal plane also allows estimation of the
amount of ovarian stroma, which has been shown to be
closely related to serum androgen level, an excess of which
is specific of PCO (reviewed in Balen et al., 2003).
In conclusion, this study confirms that measurement of
the OV yields good diagnostic accuracy to distinguish normal ovaries from PCO. However, it shows that the best
compromise between sensitivity and specificity is obtained
with a threshold set at 7 cm3, instead of the 10 cm3 threshold
proposed by the Rotterdam consensus conference on the
basis of empirical assessments. In addition, we confirm on a
different series that priority should be given to an FN >12 to
define PCO by ultrasound (Jonard et al., 2003), as proposed
by the Rotterdam consensus conference in 2003 (Rotterdam
ESHRE/ASRM-sponsored PCOS consensus workshop
group, 2004). Finally, although less used than OV, the OA
has a higher diagnostic power than OV. Whether this could
help in distinguishing PCO from MFO deserves further
studies.
Acknowledgements
We thank Mrs Lydie Lombardo and Sylvie Vanoverschelde for their
assistance in collecting the blood samples, and Miss Celine Vandaele
for her assistance in computing the clinical, biological and ultrasound
data. Supported by a grant from the Délégation à la Recherche du
CHU de Lille, France.
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Submitted on March 29, 2005; resubmitted on May 18, 2005; accepted on May
24, 2005