Systematic Sonographic Classification of Uterine Fibroids to Support Nonspecialist Infertility Investigation

Uterine fibroids, also known as leiomyomas and myomas, are benign tumors arising from the uterine smooth muscle and are one of the most common gynecological tumors in women [1]. Although uterine fibroids can be asymptomatic, patients with fibroids can present with a gamut of symptoms including heavy menstrual bleeding (HMB), urinary frequency, pelvic pain (with and without the feeling of pelvic heaviness), and infertility [2]. The term menorrhagia was abandoned and replaced by HMB by international consensus in 2007 and adapted by the Federation Internationale de Gynecologie et d'Obstetrique (FIGO) to describe one of the clinical symptoms of fibroids [3, 4]. The change was made to improve the understanding of symptoms for both the patient and clinician, as the term HMB can be translated into most languages [3]. Fibroids with severe symptoms can impact the quality of life, and women report emotional distress [2]. Uterine fibroids can be associated with poor obstetric outcomes, late miscarriage, and increased cesarean delivery [2, 5, 6]. Controversially, the impact of uterine fibroids on fertility continues to be debated; however, uterine fibroids have been reported as more prevalent in women with infertility [7-11]. Ultrasound has long been accepted as the primary form of uterine imaging due to its broad availability, cost effectiveness, and high spatial resolution [12]. From sonographic imaging alone, the number, size, and location of uterine fibroids, including their vascularity, can be clearly reported. Consistent and standardized reporting of uterine fibroids is required to enable appropriate patient management, including surgical planning where required [12]. The FIGO ultrasound classification of fibroids has been applied by the specialist ultrasound practitioner for more than 10 years. The adaptation of the FIGO classification by the nonspecialist practitioner is unknown [4]. Additionally, the adaptation of the FIGO classification in the literature is not widespread, with a more recent article describing optimization of power Doppler for the assessment of uterine fibroids not mentioning FIGO, rather referring to the Morphological Uterine Sonographic Assessment (MUSA) [13]. The original authors of MUSA refer to FIGO; however, the less experienced reader may not be aware that MUSA uses FIGO and thus may remain unaware of FIGO [14]. The aim of this paper is to describe the FIGO classification of fibroids utilizing ultrasound images and schematics to allow greater comprehension of this classification for the nonspecialist ultrasound practitioner. A pneumonic incorporating the FIGO classification has been developed to support the systematic reporting of fibroids. Systematic reporting is especially relevant in the presence of fibroids and when the clinical presentation is infertility. The possible impact of fibroids on fertility, as well as relevant uterine anatomy will also be described. Fibroid treatment options are beyond the scope of this paper and will not be discussed. The prevalence of uterine fibroids is variably reported and likely underestimated as asymptomatic patients are less likely to present for diagnosis and treatment [15-17]. It has been reported that 70% of women have fibroids while the number of women affected by fibroids in Australia and New Zealand is low [15, 16]. An estimated 7.3% of Australian women will be diagnosed with a fibroid by the ages of 45–49 years [15, 17]. In women of reproductive age, the incidence of fibroids is reported to be varied and estimated at 5.4% to 77% [15]. The highest reported risk factor for developing uterine fibroids is having a black African background, which corresponds to a two-to-three-fold increased prevalence of uterine fibroids, with a reported 80% of African American women reporting having fibroids [2, 15]. Other risk factors for developing a uterine fibroid include nulliparous women of reproductive age and women over the age of 40 years [16, 17]. A family history of fibroids and women who have given birth to children over 5 years prior also report increased prevalence of fibroids [15, 16]. In a number of studies, smoking has been reported to have a small protective effect against the development of fibroids, except in women with African background [15, 18-20] and contraceptives, whether oral or injected, can also reduce the development of fibroids. Younger and multiparous women also report a decreased incidence and prevalence of uterine fibroids [2, 15]. Although uterine fibroids have been reported to be more prevalent in women with infertility, they have not been conclusively proven to be a primary cause [7]. It has been established that fibroids are more prevalent as a woman approaches the age of 40 years and considering the trend to postpone starting a family, it is not surprising that there is a higher incidence of fibroids in women seeking infertility treatment [9, 15, 16]. The impact of fibroids on natural fertility has been insufficiently investigated [21]. However, in women seeking fertility treatment, intramural (IM) fibroids over 30 mm were found to impact live birth rates, and an IM fibroid in contact with the endometrium over 20 mm can negatively impact not only the live birth rate but also implantation and clinical pregnancy [22, 23]. Although many studies conducted relating to infertility included matched controls (no fibroids), no study to determine the impact of fibroids on natural fertility has been conducted. Transvaginal ultrasound (TVUS) and transabdominal ultrasound (TAUS) are widely acknowledged and accepted as the screening tool of choice for fibroids [24]. The usefulness of ultrasound imaging is dependent on the operator, quality of image acquisition, ultrasound system technology, and the patient [4, 24]. The ultrasound system should be of a quality where myometrial and endometrial features are clearly demonstrated and, as such, a high frequency multi-Hertz TVUS transducer is essential [4]. Along with the following recommendations, careful assessment of the uterus using TAUS and TVUS can support the determination of fibroid position, number, size, and FIGO classification. The total uterine volume should also be estimated and reported [4]. Where possible, an ultrasound system with 3D capability can provide further definition of fibroid cavity involvement. Contrast sonohysterogram (also known as sonohysteroscopy and hysterosonography) is an appropriate follow-up modality when determination of a normal endometrial cavity is inconclusive [12]. Prior to surgical treatment and less often where a lesion cannot be clearly defined, follow-up magnetic resonance imaging (MRI) and/or hysteroscopy under anesthetic can be considered [12, 25]. Internationally, there have been inconsistencies in terminology when reporting ultrasound findings related to uterine fibroids, which can lead to confusion with respect to the interpretation of ultrasound results, possibly impacting patient management. Also known as the International Federation of Gynecology and Obstetrics, FIGO developed and published a classification system for categorizing the location of uterine fibroids [4, 26]. This FIGO classification designates fibroids into 10 categories according to the position of the fibroid, to promote consistency of sonographic reporting and the universal use of terms [4]. FIGO fibroids 0–3, 8, and 2–5 are demonstrated in Figure 1a while FIGO 4–7 are demonstrated in Figure 1b with Table 1 detailing each classification aligned with historical fibroid classification to provide context for the general sonographer. When the patient is referred for screening for infertility, clear and systematic reporting of fibroids is needed using the FIGO criteria. Historically speaking, there were three fibroid classifications: subserosal (SS), IM, and submucosal (SM). While the FIGO classification now uses 10 levels of classification, fibroids historically classified as SM were assigned the FIGO designation of 0–3. These fibroids involved the endometrial cavity and were the most likely cause of symptoms such as HMB and contributing factors to infertility [4, 22]. Fibroids previously described as IM, SS, and pedunculated were not initially described but were later assigned a FIGO classification of FIGO 4–7 [4]. FIGO 8 is a fibroid not arising from the myometrium and located outside the body of the uterus such as the cervix [4]. The FIGO 2–5 fibroid is predominately IM while simultaneously involving both the endometrial cavity and uterine serosa; however, more than half the maximum diameter of the fibroid involves the myometrium [26]. Without fluid in the endometrial cavity (physiological or by sonohysterogram) it may be difficult to determine whether the fibroid extends into the cavity; however, 3D TVUS may be useful. The FIGO 2–5 fibroids are of particular interest when the patient has a desire for pregnancy and are treated similarly to FIGO 0, 1, and 2 fibroids by fertility specialists [27]. The uterus consists of three layers: serosa, myometrium, and endometrium, with the serosa as the external thin layer of peritoneum (serosa) and the mucosal endometrium being the innermost layer [28-30]. The myometrium is the smooth muscle layer primarily responsible for uterine contractions and also divides into three layers: inner, middle, and outer myometrium [29]. The junctional zone (JZ) which can be visualized in a coronal plane using ultrasound, is the innermost layer of the myometrium in contact with the endometrium and is reported to measure between 5 and 8 mm in thickness [29]. Unlike other mucosal-muscle layers, there is no basal lamina associated with the JZ [29]. By disrupting the JZ, FIGO 0–2 fibroids may impede the progression of sperm, as the natural peristalsis of the JZ is impacted by fibroids that involve the endometrial cavity [7, 8, 31]. Embryo implantation may also be inhibited due to the impact of fibroids on the JZ, and therefore FIGO 0–2 and FIGO 2–5 are of particular interest to the fertility specialist and require consistent and systematic reporting [7]. Increased uterine peristalsis has been demonstrated using cine MRI in patients with FIGO 1–4 fibroids during the post-ovulatory luteal phase (when embryo implantation is most likely) compared to women without fibroids, where in the luteal phase, peristalsis frequency is reduced [8, 32]. In a small study with 15 participants, all having IM fibroids, myomectomies were performed [32]. Pre- and post-surgical uterine peristalsis was assessed using cine MRI, and in 14 participants, uterine peristalsis was noted as normal post-myomectomy [32]. Within 8 months of the post-surgery MRI, 40% of participants conceived, with five being natural conceptions [32]. Although the JZ can be visualized in the 2D ultrasound longitudinal view, it is more easily assessed in its entirety utilizing 3D volume acquisition by translating or moving through the slices of ultrasound imaging data in the coronal plane. Figure 1c is a schematic representation of the uterus in the coronal view identifying the uterine layers and the corresponding historical fibroid designation in relation to the anatomy, with Figure 1d as the corresponding 3D rendered coronal sonographic representation of the uterus. Figure 1a–d can also be viewed in poster format as a quick reference tool in Figure S1. Increasingly, fibroids are identified in women referred with infertility; so in addition to reporting location, volume, and number of fibroids, additional information may be required [18]. FIGO 2–6 fibroids in proximity to the uterine cornu may compress the interstitial portion of the fallopian tubes, obstructing natural sperm and oocyte movement, thus hindering conception [7, 8]. In this instance, the distance of fibroids to the uterine cornu may be useful, as well as the distance from the fibroid to the endometrium, and where relevant, the distance from the serosa [7, 8]. Similarly, cervical fibroids (FIGO 8) that distort the cervical canal may inhibit sperm travel and should be noted for reporting [7-9]. Without the presence of physiological fluid in the endometrial cavity, the relationship to the uterine cavity or endometrium (FIGO 0–3) with fibroids may be more difficult to determine with 2D TVUS alone [4]. In a general ultrasound setting when a fibroid appears to be positioned wholly within the cavity, but no stalk can be identified, a FIGO 0 classification should be reported as suspected and sonohysterogram recommended. Where the fibroid is thought to be a FIGO 1 or FIGO 2 and 3D TVUS is available, the coronal plane can be assessed to determine the myometrial involvement. Equally where a FIGO 3 fibroid is suspected, again the coronal plane can be assessed to determine if the fibroid involves the endometrial cavity. The application of 3D TVUS will be discussed as a tool to determine the FIGO classification of fibroids involving (or not involving) the endometrial cavity. Where 3D TVUS is not available, a sonohysterogram should be recommended to confirm the FIGO 0–3 classification as fibroids involving the endometrial cavity are more frequently found in women investigating their infertility [7, 8, 22, 33]. Where more than four fibroids are present, those fibroids thought to be most relevant to the clinical presentation should be classified using the FIGO system, the volume reported and the proximity to endometrium, serosa, and/or uterine cornu recorded; however, local protocols should be followed [4, 7, 18]. FIGO 0 is an intracavity fibroid attached to the endometrium by a stalk (Table 1, Figure 2) [34]. Differentiating FIGO 0 from FIGO 1 using 2D TVUS alone is not possible without the presence of pathological or introduced fluid in the cavity [35]. Fluid in the cavity delineates the boundaries of the fibroid, outlining the presence of a stalk as is the case of Figure 2 (FIGO 0) where during a sonohysterogram, introduced anechoic fluid delineates the cavity, fibroid, and identifies the stalk (arrow). Aligned with the hypothesis that fibroids involved with the endometrial cavity are thought to affect the natural peristaltic action of the endometrial cavity, the stalk of the FIGO 0 fibroid is thought to impact implantation and possibly sperm progression [7, 8]. A FIGO 1 fibroid is an intracavity fibroid, attached to the myometrium with less than 50% IM (myometrial) involvement (Table 1, Figure 3). A 2D/3D TVUS will demonstrate a fibroid with a SM component (Figure 3a) however, determination of the level of myometrial involvement can be difficult. A sonohysterogram (Figure 3b) with the introduction of fluid into the cavity will demonstrate less than 50% of the maximum diameter of this fibroid with an IM component. The solid circle in Figure 3a,b approximates the fibroid, while the dotted line in Figure 3b approximates the boundary of the endometrial cavity, which is used to determine the level of the IM component. This the fibroid to be a FIGO 1 fibroid, as less than 50% involves the The FIGO 1 fibroid and the endometrial cavity and has been reported to to embryo implantation [7]. A FIGO 2 fibroid is an intracavity fibroid, attached to the myometrium with more than 50% IM (myometrial) involvement (Table 1, Figure Figure is a 2D TVUS image of an uterus an IM fibroid also involving the endometrial cavity. A 3D volume in the coronal plane (Figure more than 50% of the maximum diameter of this fibroid has an IM component this fibroid as a FIGO The solid circle in Figure the fibroid while the dotted in both demonstrate the boundary of the endometrial cavity and, the FIGO 1 fibroid, the FIGO 2 fibroid is thought to to embryo implantation [7]. A FIGO 3 fibroid is an IM fibroid with myometrial involvement but is in contact with the endometrium (Table 1, Figure Figure is a 2D TVUS image of an uterus with a IM fibroid the endometrial cavity Without the presence of fluid in the cavity, it is difficult to determine whether there is endometrial involvement. A sonohysterogram fluid and the clear of the endometrium of a endometrial thickness (Figure TVUS 3D volume acquisition and the coronal plane optimization (Figure demonstrate the fibroid the cavity. The coronal view the endometrium is not and no cavity involvement of the When sonohysterogram is not available, other 2D and 3D TVUS can be applied to determine whether the fibroid is likely to be a FIGO In Figure and utilizing 2D IM fibroids in the uterus can be in contact with the endometrium (Figure Figure is a IM fibroid while Figure is an IM 3D volume acquisition, optimization in the coronal plane (Figure no involvement of the fibroid with the cavity (Figure a FIGO 3 classification and by the 3D coronal In Figure the coronal plane view of the fibroid involvement with the cavity and is likely a FIGO 2 fibroid as more than 50% of this fibroid is IM, as in Figure When 3D TVUS is not available, 2D TVUS can be used by the uterus with a on the endometrial cavity by through the uterus in simultaneously the endometrial cavity. A cine can be and to determine whether the fibroid involves the cavity or whether the fibroid is only This is especially in the presence of fibroids and a cine of a uterus with fibroids. This cine that of the fibroids involve the endometrial cavity, and the IM fibroid be classified as a FIGO A recent and systematic FIGO 3 fibroids to be associated with fertility in patients including implantation and live birth than patients without fibroids FIGO fibroids are IM fibroids within the myometrium (Table 1, Figure FIGO fibroids can be to especially in the presence of fibroids and other uterine such as and tumors [4, Figure a fibroid wholly within the myometrium and not in contact with the cavity or Figure a fibroid also within the myometrium with no cavity and the serosa, a fibroid within the myometrium and not in contact with the serosa is as a FIGO Although not involving the cavity, FIGO fibroids over 3 have been reported to impact fertility and pregnancy and, as such, require consistent and systematic reporting using the FIGO classification The and number of fibroids are also thought to impact fertility, with fibroids thought to endometrial and myometrial and are associated with all of which continues to be due to the of [9, in Figure 8, a fibroid is classified as FIGO 5 when more than 50% of its diameter is IM and in contact with the serosa [26]. Unlike the FIGO the FIGO 5 fibroid is not in myometrium [26]. A FIGO 5 fibroid to the uterine cornu may cause of the interstitial portion of the fallopian sperm progression to the oocyte and embryo to the uterine cavity [7, Where relevant, and in the context of infertility, proximity to the uterine cornu should be reported. A FIGO fibroid is a fibroid where less than 50% of the maximum diameter of the fibroid has a myometrial (or component but the serosa is involved (Table 1, Figure The FIGO its especially when to a cine using assessment the in the is a fibroid attached to the uterus and the as This is an of a FIGO fibroid as less than 50% of the maximum diameter is Figure other of a FIGO FIGO 5 fibroids, a FIGO fibroid in the of the uterine cornu may cause of the interstitial portion of the fallopian and distance to the uterine cornu should be reported. determine a FIGO fibroid that extends beyond the the stalk be of the of the fibroid, the stalk may be difficult to when the fibroid is a TVUS described by et the uterus and can be assessed using both the transducer and in a This can support the of the as in with the corresponding image as Figure Figure a fibroid with a which is more easily The FIGO fibroid, of size, is the likely to to infertility This classification is for fibroids with no myometrial with the most likely being a cervical fibroid but also including broad fibroids and fibroids [26]. A cervical fibroid from the cervical in the and has no contact or with the endometrium or myometrium fibroids can be wholly within the cervical or involve the cervical Although fibroids can as a of and or a pedunculated however, de fibroids have been reported with no history of fibroids and/or pelvic These from pelvic fibroids are also a as they are often of and to be as from the uterus and/or on cervical fibroids is When a cervical fibroid can the cervical impacting fertility treatment, as embryo the cervical canal should be performed without the to or the which can in the presence of a cervical fibroid In the case of FIGO 8 fibroids are associated with and increased cesarean An of a cervical fibroid (FIGO 8) can be in Figure and can to fibroids from other benign and uterine Fibroid is but often following the of the fibroid as can be in Figure In a often with fibroids, and are more often and the from the endometrial cavity (Figure both and where is not a of fibroids In and are the lesion in an with the more of a fibroid In of MRI is to support between benign and uterine Figure is a 2D TVUS image of appears to be a cervical (FIGO 8) However, with the addition of as in Figure a arising from the endometrial cavity was identified attached to the fibroid, this to be FIGO 0 rather than a FIGO This classification was later at further the of This is an paper on literature with the to fibroids using FIGO for the nonspecialist sonographer. imaging and the schematics and The relationship of each to the of infertility has been so ultrasound imaging and reporting can be standardized and to the clinical The use of the pneumonic a standardized A of this is the imaging has been performed by Additionally, the to a FIGO 0 and FIGO 1 fibroid may not be possible in general without fluid in the cavity and, as such, may require to a specialist where 3D TVUS is not available, the to determine a FIGO 2 or FIGO 3 fibroid may be Where 3D TVUS is not and/or physiological fluid is not present in the cavity to the presence of a the fibroids should be reported as suspected FIGO 0–3, and sonohysterogram is recommended for and to fibroids are needed to improve and improve in categorizing fibroids according to FIGO criteria. on of FIGO be of Although fibroids involving the endometrial cavity (FIGO and can cause to uterine peristalsis and are more prevalent in women seeking treatment for infertility. FIGO 8 fibroids involving the cervix can inhibit fertility The relationship between infertility and other fibroids (FIGO is also and with and number of fibroids as well as the position in relation to the uterine anatomy thought to be contributing factors related to infertility. and consistent reporting of fibroid as the accepted FIGO classification system is for appropriate patient A systematic using the pneumonic the consistent use of terms and FIGO classification can enable the of patients seeking as to the possible impact of their fibroids on their In the of this the to for support the and for also Ultrasound for and Ultrasound for by as of the the of Australian The authors no of not to this article as no were or during the Figure of 1 and as a poster for quick by 2D TVUS in from to on the endometrium, no cavity involvement with the fibroid to the endometrium identified with an to the 2D TVUS cine in of a FIGO fibroid to the The the in and longitudinal of a pedunculated fibroid identified by the as a FIGO The is not responsible for the or of information by the than should be to the corresponding for the