Evaluation of the Uterine Causes of Female by Ultrasound: A Literature Review Shohreh Irani (PhD)1, 2, Firoozeh Ahmadi (MD)3, Maryam Javam (BSc)1* 1 BSc of Midwifery, Department of Reproductive Imaging, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, Iranian Academic Center for Education, Culture, and Research, Tehran, Iran 2 Assistant Professor, Department of Epidemiology and Reproductive Health, Reproductive Epidemiology Research Center, Royan Institute for Reproductive Biomedicine, Iranian Academic Center for Education, Culture, and Research, Tehran, Iran 3 Graduated, Department of Reproductive Imaging, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, Iranian Academic Center for Education, Culture, and Research, Tehran, Iran

A R T I C L E I N F O A B S T R A C T Article type: Background & aim: Various uterine disorders lead to infertility in women of Review article reproductive ages. This study was performed to describe the common uterine causes of infertility and sonographic evaluation of these causes for midwives. Article History: Methods: This literature review was conducted on the manuscripts published at such Received: 07-Nov-2015 databases as Elsevier, PubMed, Google Scholar, and SID as well as the original text books Accepted: 31-Jan-2017 between 1985 and 2015. The search was performed using the following keywords: infertility, , ultrasound scan, transvaginal sonography, , fibroma, Key words: leiomyoma, , intrauterine , Asherman’s syndrome, uterine synechiae, , congenital uterine anomalies, and congenital uterine Menstrual cycle malformations. Ultrasound Results: A total of approximately 180 publications were retrieved from the Uterus respective databases out of which 44 articles were more related to our topic and studied as suitable references. In addition, 11 published books on ultrasonography and infertility were evaluated to provide more precise knowledge on the mentioned areas. According to the literature, ultrasonography has a crucial role in the investigation and differentiation of uterine disorders in females with infertility. However, the diagnosis depends on the day of , clinical prese- ntations, and the suspected uterine disorder. In this review, we provided the key notes about proper timing of the ultrasound examination. Conclusion: Ultrasonography is the first step imaging tool in the investigation of female infertility, which provides information for the diagnosis of uterine disorders. However, the accurate diagnosis depends on the “time of evaluation”. Therefore, every midwife needs to learn about the “optimum timing” for ultrasound evaluation based on each patient.

Please cite this paper as: Irani Sh, Ahmadi F, Javam M. Evaluation of the Uterine Causes of Female Infertility by Ultrasound: A Literature Review. Journal of Midwifery and Reproductive Health. 2017; 5 (2): 919-926. DOI: 10.22038/jmrh.2017.8252

Introduction Infertility is a widespread phenomenon that account for about 3% of the infertile women and affects approximately 10-15% of the couples is categorized in seven classes, which will be around the world (1, 2). There are several described in details later (1-5). congenital or acquired uterine disorders, which Sonography is known as the first imaging cause infertility in the females. The acquired modality in the investigation of the female uterine abnormalities that are responsible for to detect the mentioned disorders among the female infertility include polyps, some types of infertile females. It is an “accurate, non-invasive, fibromas, adenomyosis, and some endometrial and cost-effective” modality, which provides disorders such as intrauterine adhesions. On the useful knowledge for the detection and other hand, the congenital uterine anomalies characterization of the possible female infertility

* Corresponding author: Maryam Javam, Graduated, Department of Reproductive Imaging, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, Iranian Academic Center for Education, Culture, and Research, Tehran, Iran. Tel: 9774066673; Email: [email protected]

Irani Sh et al. JMRH Uterine Factors of Infertility factors (1, 2, 4-6). All infertile women undergo as the original text books between 1985 and 2015 an initial ultrasound pelvic exam (baseline were employed. A careful search was performed sonography) to investigate the probable causes using the following keywords: “infertility”, of infertility. A careful pelvic ultrasound, “uterus”, “ultrasound scan”, “transvaginal particularly transvaginal sonography (TVS), can sonography”, “endometrial polyp”, “fibroma”, detect the uterine abnormalities, ovarian “leiomyoma”, “endometrial hyperplasia”, “intrau- disorders, and other pathologic conditions, terine adhesions”, “Asherman’s syndrome”, which lead to female infertility (1,2,4-8). “uterine synechiae”, “adenomyosis”, “congenital Therefore, it can help the midwives, physicians, uterine anomalies”, “congenital uterine gynecologists, and infertility experts to examine malformations”, and “timing+ultrasound scan”. the infertile women and make better treatment The articles, which were written in English or choices for these patients. Persian and contained helpful data on “diagnostic Hackeloer examined the role of ultrasound in criteria of uterine disorders on transvaginal investigation and management of female ultrasound scan” and “proper timing of the infertility in a review article in 1984. He ultrasound examination” were considered as precisely described the uterine abnormalities, proper references. All manuscripts were carefully ovarian disorders, and adnexal masses, which assessed, and the proper articles were selected to cause infertility using ultrasound images (9). be studied. The irrelevant articles or those Recently, Hrehorcak and Nargund (2011) have written in other languages were excluded from published a review study on the new the study. perspective of diagnosing female infertility by Finally, a total of approximately 180 advanced ultrasound techniques (10). There are manuscripts were carefully assessed. Out of a number of reviews targeting this issue, these, 12 articles were not published in English however, all of them are written by radiologists or Persian, 16 manuscript provided diagnostic and gynecologists and provide advanced and criteria for instead of TVS, 30 specific knowledge for the specialists. articles provided diagnostic accuracy of TVS To the best of our knowledge, no study has instead of diagnostic criteria, and 78 papers did been published in this area for the midwives. not discussed about the timing of the ultrasound Since many midwives work at the infertility scan. Therefore, 136 manuscripts were not treatment centers or personal offices, they thoroughly related to the topic of interest and interface with infertile females and need to excluded from the study. The remained 44 involve in the infertility assessment. Ultrasound articles met the inclusion criteria and were scan is one of the most used diagnostic tools for studied as suitable references. In addition, 11 the infertility workup. Therefore, every midwife books on ultrasonography and infertility were needs to learn about the application of the evaluated to provide more precise knowledge on ultrasound and management of the patients the investigated areas (Figure 1). based on abnormal findings. Nevertheless, there are not enough learning opportunities for Results midwives in this area. With this background in We gathered the useful findings of the mind, the present study aimed to provide useful reviewed studies on uterine causes of female practical knowledge about the ultrasonography infertility and the key points on the diagnosis assessment of female infertility and give a good of these causes by ultrasonography, which chance to midwives to further learn about this were as follows issue. Acquired abnormalities Materials and methods Polyps This literature review was conducted on the Endometrial polyps are benign localized articles investigating the diagnosis of uterine overgrowth glands, vessels, and stroma causes of infertility by means of ultrasound scan. within the uterine cavity (1, 3, 11, 12). They The articles published in such databases as mostly originate from the fundal region and PubMed, Elsevier, Google Scholar, and SID, as well extend to the internal os and may be seen single

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Uterine Factors of Infertility JMRH Irani Sh et al. or multiple. Their size differs from a few nevertheless, they commonly cause abnormal millimeters to centimeters and may be sessile or and infertility (11, 12, 15). The pedunculated (1, 11). There are some risk factors management of the females with endometrial recognized to cause polyps, including age, polyps depends on the symptoms, fertility issues, hypertension, obesity, and tamoxifen use; and risk of malignancy (1). Polypectomy by means however, the definite cause of polyps is unknown. of hysteroscopy is considered as an effective and The symptoms do not depend on the size, safe gold standard for both diagnosis and number, or location of the polyps (11-15). treatment of this condition, especially in case of Polyps are most often asymptomatic; infertility treatment (11, 14, 16).

Figure 1. Study design

TVS is identified as the best diagnosis tool in age, family history, ethnicity, weight, diet, this regard; however, it is better to be performed smoking, pregnancy, and hormone replacement before day 10 of the cycle to decrease the risk of therapy (18-21). false-positive and false-negative findings (1). Fibromas, which are also known as myomas, Regarding this, days 4-6 are preferred (17) since leiomyomas, and fibroids, arise within the uterine the has its thinnest thickness during , nevertheless, they may be some- this period (1, 11, 17). It is important to note that times detected in the , ovaries, or broad sonography needs to be performed by an ligament. Fibromas are classified into three groups experienced sonographist because differentiation based on their location: (1, 3, 18-20, 22, 23). of polyps from the clot, synechiae, submucosal 1. Intramural fibroids are the most prevalent fibroid, and hyperplasia must be considered for types, located within the myometrium and correct diagnosis (17). totally surrounded by it. 2. Subserosal fibroids are externally extending to Fibromas the serosa, which can pass to the pelvic cavity Fibromas are benign tumors of the uterus, and make a “pedunculated uterine fibroma” which mostly originate from smooth muscle. within pelvic cavity. However, they may contain various amount of 3. Submucosal fibroids grow into the endometrial fibrous connective tissue (3, 18-21). They are cavity; they are the least common, but the most the most common pelvic masses among the significant type due to causing more symptoms reproductive aged women, which is found in 20- and infertility. 40% of these population (18, 19). Although the Myomas can be found either solitary or exact cause of this condition is unknown, these multiple, ranging in size and location (19). As a tumors are hormone-related and respond to result, regarding the symptoms, they differ from both estrogen and progesterone. However, being asymptomatic to having severe symptoms several possible risk factors are raised, including such as infertility. The usual manifestations of

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Irani Sh et al. JMRH Uterine Factors of Infertility myomas entail abnormal uterine bleeding, pelvic various size and shape, which results in pressure or pain, , and urinary thickened endometrium (15, 31-34). It occurs symptoms (3,18-20,23-26). Infertility may following the excess unopposed estrogen occasionally be observed, which is most often stimulation of any source (31, 33). Polycystic caused by submucosal fibroids. Furthermore, ovarian syndrome patients are more likely to recurrent miscarriages are shown to be relevant to have hyperplasia due to higher circulating uterine fibroids (19, 27, 28). estrogen levels. Therefore, a careful endometrial Additionally, some researchers indicated that measurement should be performed in this group the probability of the in vitro fertilization failure or during the infertility workup. Endometrial pregnancy loss in the patients with distorted hyperplasia is suspected in women presenting endometrium due to myomas, increases up to 50% with heavy, prolonged, frequent, and irregular (19). Therefore, the accurate investigation of uterine bleeding (31-35). fibromas prior to infertility treatment is essential. When evaluating these patients by TA/TV The treatment choices vary from expectant sonography, we should note that the endometrial management to medical and surgical therapy (e.g., thickness and appearance change cyclically due myomectomy or hysterectomy), depending on the to different phases of menstrual cycle. Therefore, patient’s age, symptoms, and reproductive we should ask about the day of the cycle in which expectation (3,19,29,30). The recurrency may the sonography examination was performed. happen; nevertheless, the likelihood of malignancy Endometrial hyperplasia will be detected if the is rare (19). endometrial thickness measures ≥ 8 mm during TVS and transabdominal sonography (TAS) the proliferative phase, ≥ 16 mm during the are the primary imaging methods used in the secretory phase, and ≥ 5 mm during the investigation of female pelvis, and the technique menopause (35-39). of choice in the evaluation of uterine myomas (1, 3, 19). In experienced hands, the sonographic Intrauterine Adhesions examination facilitates the detection of the Intrauterine adhesion (uterine synechiae, amounts, types, location, and size of the IUAs) is described as the presence of fibrotic tissue fibromas as well as the amount of endometrial within the endometrial cavity, which causes distortion due to myomas, which is very intracavitary adhesions (1, 40-42). It is an important in the infertility workup. Therefore, acquired condition resulted from trauma to the these points should be considered in basal layer of the endometrium usually following sonography reports. It’s worth noting that in curettage or infection. Adhesions range from case of small fibromas of less than 5 mm in minor synechiae to severe cohesive adhesions diameter or in obese patients, the TVS would be (Asherman’s Syndrome) (1, 40-45). The most more accurate and sensitive than the TAS. common complications associated with IUA are In case of submucosal fibroid and suspected , infertility, recurrent , and endometrial distortion, it may be difficult to preterm birth (45, 46). differentiate myoma from polyp. Consequently, IUA is detected by sonography when the further imaging modalities, such as sonohy- endometrium is thin and irregular (1). However, sterography or tree-dimensional (3D) sono- the experts believe that TVS has limited use in graphy, are required for detailed investigation. confirming adhesions (47, 48). Extra imaging by The endometrial thickness has a vital role in the means of hysterosonography may be helpful in accurate investigation of myomas by 3D TVS. this regard (47). To confirm the diagnosis, the The optimum timing of sonographic assessment endometrium needs to be assessed after taking of myomas in this situation is when the preoperative exogenous estrogen for 4-8 weeks to endometrium is more than 5 mm in diameter (1, measure maximal endometrial thickness (47-49). 18, 19). Adenomyosis Endometrial Hyperplasia Adenomyosis is a common benign condition in Endometrial hyperplasia is defined as an which ectopic endometrial glands grow into the abnormal proliferation of endometrial glands of uterine myometrium (3, 36, 50). As a result,

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Uterine Factors of Infertility JMRH Irani Sh et al. myometrial hypertrophy is associated with this During the sixth week of gestation, the uterus, disorder (48). It often occurs in the multiparous cervix, and uterine tubes are developed from a pair women. There are several possible risk factors for of mullerian ducts (paramesonephric), which is this condition including uterine trauma, , associated with the improvement of three phases, chronic , and hyperestrogenism. The namely organogenesis, fusion, and septal clinical manifestations of adenomyosis are pelvic resorption (51, 54). In the organogenesis phase, pain, , menorrhagia, menome- the constitution of both mullerian ducts occurs and trorrhagia, uterine tenderness and enlargement, as a failure in this regard results in uterine well as infertility (36, 50). agenesis/hypoplasia or a unicornuate uterus. The The TVS is the first step imaging modality for fusion phase is described as the fusion of the ducts the evaluation of the women suspected to have to constitute the uterus and any defect in this adenomyosis. Accordingly, several studies have phase leads to a bicornuate or didelphys uterus. indicated that TVS has a high sensitivity and The final phase is characterized as the further accuracy in the diagnosis of adenomyosis, resorption of the central septum once the ducts compared to the magnetic resonance ima- have been fused. If there is any deficiency in this ging (MRI). However, TVS is a skill-dependent tool stage, a septate uterus will be the result (51, 53). and the final diagnosis may need to be confirmed The accurate diagnosis of uterine abnormalities is by MRI in cases that are uncertain (50). crucial because the treatment procedures and Adenomyosis should be considered if the following pregnancy outcomes differ between the various phrases are reported by the sonographist: 1) A classes of malformations (52). normal-sized or enlarged globular shaped uterus, Sonography, in combination with hysteron- 2) A heterogeneous mottled texture of the salpingography, has an important role in the myometrium, 3) “Swiss cheese appearance” due to investigation and classification of the uterine blood clots within the myometrium, 4) Indistinct anomalies. In case of no clinical doubt regarding endometrial line due to disrupted border between the tubal disorders, TVS can be applied as a more the endometrium and myometrium (36, 50). tolerable and less invasive imaging modality. The combination of 3D techniques with TVS gives the Congenital Anomalies specialist the opportunity to investigate the Uterine malformations are a various group of coronal view of the uterus, which configures both congenital uterine anatomic abnormalities endometrium and myometrium together for more originated from the development defect of accurate diagnosis. mullerian ducts during fetal development (51-53). We should note that the optimum timing of They are associated with higher incidences of ultrasound evaluation and the classification of infertility, recurrent abortions, intrauterine fetal anatomical uterine disorders are “the secretary death, intrauterine growth retardation, pre- phases of menstrual cycle” when the endometrial mature delivery, fetal malposition, caesarean thickness and echo pattern are better section, retained placenta (51-55), and such characterized (1, 53-55). These anomalies are gynecological complications as and evaluated at days 11-14 and 17-21 in routine 2D (54). Uterine anomalies are ultrasound scan of the pelvis and 3D/4D detected in approximately 1-3% of all women sonography, respectively. (51); however, 10-25% of the women seek infertility workup (52). Discussion According to the American Fertility Society According to the findings of the reviewed classification, these malformations are classified articles, uterine polyps are best distinguished into seven categories as follows (51, 52, 54): class I during days 4-6 of the menstrual cycle. includes and agenesis; class II Endometrial distortion caused by uterine fibromas contains unicornuate uterus; class III entails is well-assessed on days 11-14 and 17-21 on 2D ; class IV consists of bicornuate and 4D ultrasound imaging. Endometrial uterus; class V is septate uterus; class VI includes hyperplasia is best recognized at proliferative arcuate uterus; and class VII entails the phase. Furthermore, the congenital malformations diethylstilbestrol-related anomalies (52-54). of the uterus are best evaluated during days 11-14

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Irani Sh et al. JMRH Uterine Factors of Infertility and 17-21 on 2D and 4D sonography, respectively. of female infertility: instruction for midwives and In addition, IUA should be diagnosed by serial nurses. International Journal of Fertility and Sterility. ultrasound scans. Considering these points is 2014; 8(Supp 1):280. crucial for referring the infertile patients for 5. Singh K, Malhotra N. Step by step ultrasound in infertility. New York: McGraw-Hill; 2004. ultrasonography. 6. Derchi LE, Serafini G, Gandolfo N, Gandolfo NG,

Martinoli C. Ultrasound in gynecology. European Conclusion Radiology. 2001; 11(11):2137-2155. Sonography is an accurate, non-invasive, and 7. Irani S, Ahmadi F, Javam M. Application of cost-effective imaging modality for examining the sonography in infertility treatment cycles: infertile women. It usually provides beneficial instructions for midwives and nurses. Iranian information about the uterine disorders, which Journal of Reproductive Medicine. 2015; 1(2):36. cause female infertility. Therefore, every midwife 8. Irani S, Javam M, Ahmadi F. Correct scan, for the needs to learn about the application of this correct patient, at the correct time: a guideline for sonographic evaluation of the infertility for diagnostic imaging technique. It is worth noting midwives and nurses. Iranian Journal of that the pelvic organs are affected by cyclic Reproductive Medicine. 2014; 12(Suppl 1):127. changes during the menstrual cycle and hormone 9. Hackeloer BJ. The role of ultrasound in female therapy. Regarding this, the pathologic conditions infertility management. Ultrasound in Medicine & of pelvis need to be well-assessed depending on Biology. 1984; 10(1):35-50. the day of the menstrual cycle. Therefore, the 10. Hrehorcak M, Nargund G. “One-Stop” fertility optimal timing of the ultrasound scan is the key assessment using advanced ultrasound technology. point for the diagnosis and decision making about Facts, Views & Vision in ObGyn. 2011; 3(1):8-12. these patients. 11. Salim S, Won H, Nesbitt-Hawes E, Campbell N, Abbott J. Diagnosis and management of To the extent of the researchers’ knowledge, no endometrial polyps: a critical review of the article has investigated the female infertility literature. Journal of Minimally Invasive diagnosis by ultrasound for midwives. This article Gynecology. 2011; 18(5):569-581. would be a helpful reference for the midwives 12. Berridge DL, Winter TC. Saline infusion working in the field of infertility and all medical sonohysterography. Journal of Ultrasound in students who are interested in this area. Medicine. 2004; 23(1):97-112. 13. Machtinger R, Korach J, Padoa A, Fridman E, Zolti M, Acknowledgements Segal J, et al. Transvaginal ultrasound and diagnostic Hereby, we would like to express our gratitude hysteroscopy as a predictor of endometrial polyps: risk factors for premalignancy and malignancy. to the staff of the sonography unit at the International Journal of Gynecological Cancer. 2005; Reproductive Imaging Department of Royan 15(2):325-328. Institute for their warm cooperation. We are 14. Sharma M, Taylor A, Magos A. Management of grateful to Zahra Arianfar and Mansoureh endometrial polyps: a clinical review. Reviews in Soleimani in particular. We specially thank Narges Gynaecological Practice. 2004; 4(1):1–6. Bagheri Lankarani (PhD) for her worthy 15. Davis PC, O'Neill MJ, Yoder IC, Lee SI, Mueller PR. comments regarding the article revision. Sonohysterographic findings of endometrial and subendometrial conditions. Radiographics. 2002; Conflicts of interest 22(4):803-16. 16. Bettocchi S, Achilarre MT, Ceci O, Luigi S. Fertility- The authors declare no conflicts of interest. enhancing hysteroscopic surgery. InSeminars in

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