British Journal of Radiology 75 (2002),9-16 © 2002 The British Institute of Radiology
Polycystic ovaries
K Lakhani, MSc1,
A M Seifalian, MSc, PhD2,
W U Atiomo, MD, MRCOG3 and
P Hardiman, MD, FRCOG3
1Ultrasound Department, X-Ray, North Middlesex Hospital, Sterling Way, Edmonton, London N18 1QX and 2University Department of Surgery and 3University Department of Obstetrics and Gynaecology, Royal Free and University College Medical School, Pond Street, London NW3 2PF, UK
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Abstract
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Transvaginal ultrasound is currently the gold standard for diagnosing polycystic ovaries. The results of studies using ultrasound suggest a prevalence in young women of at least 20%. Between 5% and 10% of these women with polycystic ovaries shown on ultrasound will have the classical symptoms of polycystic ovary syndrome such as infertility, amenorrhoea or signs of hirsutism and obesity, as originally described by Stein and Leventhal in 1935. However, the significance of polycystic ovaries in asymptomatic women is still under investigation, as is the role of Doppler (pulsed and colour) and three-dimensional ultrasound. Ultrasound has also contributed to our understanding of the local and systemic haemodynamic changes associated with polycystic ovaries, although the relationship of these changes to morbidity and mortality is unknown.
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Introduction
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The condition now known as polycystic ovarian syndrome (PCOS) was first described by Stein and Leventhal in 1935 [1] as comprising amenorrhoea, hirsutism, obesity and sclerotic ovaries. It is one of the most common human endocrinopathies, affecting 5–10% of women of reproductive age [2]. The diagnosis of PCOS was previously based on a combination of clinical and endocrine features, including raised serum concentrations of luteinizing hormone (LH), testosterone (T) and androstenedione and reduced levels of sex hormone binding globulin [3, 4]. With the introduction of pelvic ultrasound in the 1980s, non-invasive assessment of ovarian morphology became possible. Ultrasound studies have demonstrated that approximately 20% of young women have polycystic ovaries (PCO) [5, 6], of whom around 25–70% have symptoms of infertility, menstrual irregularity or hirsutism, consistent with the diagnosis of PCOS [2, 5, 6]. However, the finding of PCO on ultrasound does not per se warrant such a diagnosis. More recently, high frequency transvaginal ultrasound (TVS) has superseded transabdominal (TA) real-time scanning in the diagnosis of PCO because of its superior resolution, whilst three-dimensional (3D) imaging and colour Doppler blood flow studies have allowed detailed evaluation of the stroma. The aim of this review article is to address the development of diagnostic ultrasound criteria of PCO with successive advances in ultrasound technology and to identify its salient associations.
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Developments in ultrasound imaging
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With advances in technology, in particular that of TVS, ultrasound has replaced laparotomy andX-ray pelvic pneumogynaecography in the diagnosis of PCO [7, 8]. The static B-scanners of the mid 1960s allowed visualization of ovarian enlargement as well as of cysts measuring greater than 1 cm in diameter [9]. The poor resolution of the ultrasound equipment used in the early 1970s permitted visualization of the ovarian outline only, and the diagnosis of PCO was based upon increased maximum length (>4.0 cm). However, the use of a single dimension may lead to false positive results when the full bladder compresses the ovary, or false negative results when the ovaries are spherical in shape. In fact PCO tend to be more spherical in shape so that the sphericity index (expressed as ovarian width to ovarian length ratio) is greater than 0.7 in PCO. A decreased uterine width to ovarian length ratio of greater than 1.0 has also been reported in the diagnosis of PCO. All these features are now used less frequently because of their low sensitivity [10]. Thereafter, the development of grey scan equipment in the 1970s and real-time sector scanners in the 1980s improved resolution and, for the first time, cysts less than 1 cm could easily be recognized [11]. In 1981, Swanson et al [11] described PCO as enlarged and rounded, with a mean volume of 12 cm3 and containing an increased number of small follicles (2–8 mm) encircling the ovarian cortex. However, the importance of ovarian size in diagnosis has lessened as various groups [12–14] have shown a considerable overlap between PCO and normal ovaries and as the upper limit of normal has decreased from greater than 10 cm3 to 5.5 cm3 [15]. This decrease may also reflect the broader inclusion criteria in the latter studies compared with Swanson et al who only included patients with enlarged ovaries and classic Stein–Leventhal syndrome at the extreme end of the clinical spectrum.
In 1985, Adams et al [16] published new criteria based on TA ultrasound, which required 10 or more cysts of 2–8 mm in diameter arranged peripherally around an echo dense stroma. However, these criteria have remained in widespread use even after the introduction of TVS a decade later. The high resolution of the technique allows visualization of follicles less than 5 mm in diameter as well as echogenic stroma (Figure 1
), which corresponds closely to the characteristic histopathological changes (Figure 2), and this is now accepted as the gold standard for diagnosis of PCO (Table 1). There have been at least four definitions of PCO using TVS. The most recent criteria were defined by Fox [17] and Atiomo et al [18]. These criteria differ slightly in the number of follicles and their size. However, Fox does not stipulate that the requisite numbers of follicles are seen in a single plane of the ovary. In clinical practice the ultrasonographer forms an impression of the ovary from the images obtained in three planes. Therefore, there is still a degree of subjectivity in this diagnosis. The ultrasound diagnostic criteria of PCO have been refined with advances in technology. Diagnostic accuracy has evolved from increased ovarian length to the recognition of the distribution of follicles and textural changes in the ovarian stroma. The most consistent feature of PCO, which is not seen in a normal cycling ovary, is the presence of small follicles around an echodense ovarian stroma, although recognition of the latter is highly subjective and depends upon equipment settings.
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Figure 1. Transvaginal image of a polycystic ovary showing peripheral distribution of follicles (arrows).
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Figure 2. Stained longitudinal section of a polycystic ovary showing numerous small peripheral follicles.
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3D ultrasound
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To avoid the difficulties in outlining or measuring ovarian size, 3D ultrasound has been proposed using a dedicated volumetric probe or a manual survey of the ovary [19]. 3D ultrasound has been used to measure ovarian and stromal volumes, providing information that is not available from two-dimensional (2D) ultrasound [19]. Data are transferred to a computer and can be analysed later. From the stored data, measurements can be made from the image that is reconstructed and the ovarian and stromal volumes are displayed on the screen in three adjustable orthogonal planes; subsequently the volume can be more accurately evaluated. In a study by Kyei-Mensah et al [19], the difference in ovarian size was accounted for by the differences in stromal volumes, there being no differences in follicular volume between normal ovaries and PCO. However, 3D ultrasound is governed by the same principles as 2D ultrasound and hence its resolution is reduced in obese women. Expertise and experience is therefore important, as numerous volume measurements of sufficient quality may be necessary to permit meaningful analysis.
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Doppler ultrasound
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Transvaginal colour and pulsed Doppler ultrasound in combination with B-mode imaging is used as a non-invasive method to assess blood flow in both obstetrics and gynaecology. Colour or power Doppler allows detection of the uterine and ovarian vessels as well as the network within the ovarian stroma; power Doppler is more sensitive to slow flow and allows the detection of blood flow within the ovarian stroma [20]. However, power Doppler does not as yet allow quantitative measurement of blood flow. The spectral Doppler assessment of vascular changes in the ovarian and uterine arteries in women with PCO has improved our understanding of the pathogenesis of this common condition and provides an additional variable to the traditional endocrinological and more recent ultrasound features for its diagnosis.
Colour Doppler allows the ovarian artery to be identified at the lateral border of the ovary as well as the ascending branch of the uterine artery at the cervicouterine junction [21]. This technique has been used to study the haemodynamic changes in the uterine and/or ovarian arteries during the menstrual cycle in women with normal ovaries [21]. Battaglia et al [20] reported a higher uterine artery pulsatility index (PI) in women with PCOS and a decreased resistance index (RI) within the ovarian stroma in PCOS (suggestive of increased downstream resistance) and a positive correlation with LH levels. The capillary area increases after the LH surge, causing an increase blood flow attributed to vasodilatation and resulting in flow detection with Doppler ultrasound [22]. However, using colour Doppler and spectral waveform analysis we did not find any significant differences in the ovarian artery PI or RI in PCO/PCOS women compared with women with normal ovaries (unpublished data). The mechanism responsible for these haemodynamic changes in PCOS is not known, but it may be significant that stromal blood flow in PCO (Figure 3) has been attributed to increased concentrations of serum vascular endothelial growth factor [23]. The clinical significance of these changes is also under investigation and it is of interest that a higher uterine artery PI has been associated with lower conception rates during embryo transfer in in vitro fertilization [24].
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Figure 3. A typical flow velocity diagram at the stroma shows higher velocity in a 35-year-old polycystic ovary syndrome patient.
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MRI
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Data on MRI for PCO is still limited [25]. MRI allows easier localization of the ovaries because of its multiplanar scanning of the pelvis. The image quality of MRI is improved by the use of a pelvic dedicated phased array coil receiver. The most useful planes are transverse and coronal and the T2 weighted sequence is best for assessing ovarian morphology as the cysts are displayed as high signal (white) and the stroma as low signal (black) (Figure 4). T1 weighted sequences are less informative, although following gadolinium injection there is enhancement of the stroma, suggesting that the stroma is highly vascularized in PCO. The external features of PCO (increased ovarian volume, increased roundness index (ovarian width/ovarian length ratio) and decreased uterine width to ovarian length ratio) are easily recognized on transverse cuts. Although the T2 weighted sequence displays the increased number of follicles, their detection is less easy than with ultrasound because of the poor resolution of MRI, unless using high magnetic fields of 1–1.5 T. In clinical practice, MRI is rarely used for the diagnosis of PCO as it does not provide any more information than TVS and is also an expensive modality [25]. It may be helpful in difficult situations when ultrasound either is not possible or is unhelpful (in virgin or obese women, respectively).
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How PCO differ from multifollicular ovaries
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Multifollicular ovaries (MFO) were first described by Adams and colleagues in 1985 [16], and are encountered in mid to late normal puberty, hyperprolactinaemia, hypothalamic anovulation and weight-related amenorrhoea. They differ fromPCO, having fewer cysts (6–10 per ovary; Figure 5), which tend to be larger (up to 10 mm in diameter) and distributed throughout the ovary with no stromal hypertrophy [16]. MFO result from incomplete pulsatile gonadotrophin (GnRH) stimulation of ovarian follicular development [26]. Furthermore, MFO resume a normal appearance following weight gain or treatment with pulsatile GnRH, whilst PCO retain their appearance throughout reproductive life, irrespective of time of cycle, pregnancy or drug treatment [26], and women with MFO have normal levels of LH andT and reduced levels of follicle stimulating hormone (FSH) compared with women with PCO [27].
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Pelvic pain and PCO
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Cystic ovaries have also been described [28] in women with venous congestion resulting in pelvic pain (Figure 6). This condition is thought to arise from abnormal relaxation of the pelvic veins and may respond to progesterone therapy. Adams and co-workers [29] evaluated ovarian morphology using TA ultrasound in 55 women with chronic pelvic pain and reported that women with chronic pelvic pain due to venous congestion not only had a larger uterus and thicker endometrium compared with age- and parity-matched controls but also had cystic ovaries. Of these women, 56% had cystic changes, which ranged from the classic polycystic pattern to the appearance of clusters of 4–6 cysts.
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Figure 6. Pelvic venous congestion in a young woman with polycystic ovary syndrome (for details see text).
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Early pregnancy loss
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Early miscarriage has been associated with increased LH [30] and increased T [31] levels (both of which are in turn associated with PCOS). The prevalence of early pregnancy loss ranges from 20–40% [32, 33] in women with PCOS following treatment for anovulation. Studies have shown a clear relationship between the raised serum LH level often found in women with PCOS and early pregnancy loss [34]. Because of the presumed link between PCOS and early pregnancy loss in induced cycles, the relationship between PCO and early miscarriage in women with spontaneous ovulatory cycles was studied in 56 women with three or more miscarriages. This study showed that 82% of women had ultrasound appearances of PCO [33]. However, a recent study found no increase in miscarriage rate in women with polycystic ovary morphology and a history of early embryo loss compared with women with the same history but normal ovarian morphology on ultrasound [35].
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Are PCO present in post-menopausal women?
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The clinical diagnosis of PCOS is conventionally restricted to pre-menopausal women; conversely, histopathologists do not usually identify PCO in post-menopausal women. However, in a cross-sectional study of 18 post-menopausal volunteer women and 94 post-menopausalwomen who had undergone coronary angiography, Birdsall and Farquhar [36] identified PCO in 8/18 of the volunteer group and 35/94 women in the angiography group. Moreover, the women with PCO had increased serum concentrations of T, a feature of PCO in young women. The results of this study raise the possibility that the morphological and endocrine features of PCOS may not resolve at the time of the menopause and thus highlight the need for long-term longitudinal data.
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PCO in asymptomatic women
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PCO are not confined to women with the classical symptoms of the syndrome described by Stein and Leventhal [1]. On the contrary, with the advent of TVS, PCO are commonly seen in asymptomatic women. In a study of hospital staff volunteers using TA ultrasound, the prevalence of PCO was 23% [6]. Three further studies have shown a prevalence of between 16% and 33% [5, 37, 38]. At present, however, the clinical significance of PCO in asymptomatic women is unclear, although there is evidence of biochemical abnormalities in these women similar to those present in PCOS, but to a lesser degree. In 1977, Carmina et al [39] reported LH and androgen levels between those found in normal subjects and those found in patients with PCOS. Similarly, we found a linear trend in ultrasound and endocrine variables from controls through PCO to PCOS [40].
The relationship between ovarian morphology and symptomatology is further complicated by the assertion that some women with classical symptoms of PCOS may have normal ovaries on ultrasound. One study of five women with clinical features of PCOS and cystic ovaries and five women with clinical features of PCOS and normal ovaries on TVS reported no significant endocrine differences between the two groups [41].
Although obesity was included in the original description of the syndrome [1], not all women with PCOS are obese. Obesity itself can lead to many changes ascribed to PCOS, thus it may be possible that obesity unmasks or even potentiates the endocrine changes of asymptomatic women with PCO to PCOS.
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The unilateral polycystic ovary
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The development of TVS has also identified a small group of women with one polycystic ovary in whom the contralateral ovary can be clearly visualized and appears normal. In 1999, in an observational study of 16 women with unilateral PCO and 20 women with bilateral PCO, Battaglia and co-workers [42] reported that the women in the latter group had higher concentrations of androstenedione and LH to FSH ratios. Furthermore, in women with unilateral PCO, grey scale and Doppler ultrasound showed different features in the affected and the unaffected ovary, similar to the appearance of the polycystic and the normal ovary, respectively [42].
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Wider health implications of PCOS
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PCOS is common among women of reproductive age and in clinical practice these women are seen for three major reasons: infertility (74%), menstrual irregularity (66%) and androgen excess (48%). PCOS should no longer be considered a purely gynaecological condition, as many of these women may be at an increased risk of cardiovascular disease in later life [43–45] owing to the associated risk factors of obesity, insulin resistance, hypertension and altered lipid profiles often observed in these women [46]. Using risk model analysis, Dahlgren et al [45] has estimated a 7.4-fold increase in mortality, however in the only follow-up study cardiovascular mortality was not increased [47]. The reason for this discrepancy is unknown, but it has been suggested that protective mechanisms may be operative or that this cohort was in some way not representative of the general population with PCO.
Haemodynamic changes have also been reported in women with PCOS. Prelevic et al reported lower flow over the aortic arch [48], higher resting forearm flow during reactive hyperaemia and lower incremental forearm flow [49] in PCOS than in age-matched control women. In a study using Doppler ultrasound, we found reduced PI and back-pressure (a better indicator of interpreting the PI in low impedance vascular beds such as thecerebral circulation [50, 51]), suggestive of reduced vascular tone in the internal carotid artery in women with PCOS and PCO compared with young healthy controls. These differences were independent of blood pressure, insulin resistance and other endocrine and metabolic factors [40]. In a subsequent study we reported a paradoxical constrictor response to 5% carbon dioxide (a known cerebrovasodilator) in the internal carotid artery in women with PCOS compared with women with normal ovaries [51]. We are currently investigating the possibility that this represents an abnormality in endothelial function in women with PCO. Interestingly, Lees et al [52] reported a constrictor response to transdermal glyceryl trinitrate (a potent vasodilator), which acts through the endothelial nitric oxide system in women with PCO. The clinical significance of these changes in the cerebral circulation requires further investigation, but they are indicative of widespread changes in cardiovascular function in these women, which may influence morbidity and mortality.
Although it is not quite clear whether the estimated risk of health problems in women with PCOS actually translate into long-term morbidity and/or mortality, asymptomatic women with PCOmust indeed have an increased likelihood of adverse health outcomes as a result of their PCO status. As clinicians it is ethical to advise and suggest that women with PCO/PCOS (especially the obese ones) lose weight and adopt healthy life-style practices that could reduce their risk of developing hypertension, non-insulin dependent diabetes mellitus (NIDDM) and the associated cardiovascular consequences.
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Conclusion
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The ultrasound criteria for diagnosing PCO have evolved from simply increased dimensions to the recognition of a characteristic follicular pattern and textural changes in the ovarian stroma. 3Dultrasound, together with pulsed and colour/power Doppler ultrasound, have also been used to visualize PCO, but their clinical role is not yet established. Using TVS scanning and applying strict criteria, the prevalence of PCO in the female population is at least 20%, although only between one-quarter and one-half of these women have the classic symptoms of the syndrome. The significance of this finding in asymptomatic women is currently under investigation. Women with clinical features of the syndrome are at increased risk of developing NIDDM, but concerns about cardiovascular risks have not yet been clearly confirmed. Ultrasound is also being used to identify systemic haemodynamic changes in these women, but the clinical significance of these changes and the mechanisms responsible have yet to be established.
Received for publication June 11, 2001.
Revision received September 25, 2001.
Accepted for publication October 16, 2001.
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Abstract
Introduction
