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12 Intrauterine Adhesions
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25. Onah HE, Ezike HA, Mgbor SO. Saline sonohystero­salpingographic fi ndings in infertile Nigerian women. J Obstet Gynaecol. 2006;26(8):788–90.
26. Kowalczyk D, Guzikowski W, Więcek J, Sioma­Markowska U. Clinical value of real time 3D sono­hysterography and 2D sonohysterography in comparison to hysteroscopy with subsequent histo­pathological examination in perimenopausal women with abnormal uterine bleeding. Neuro Endocrinol Lett. 2012;33(2):212–6.
27. Soares SR, Barbosa dos Reis MM, Camargos AF. Diagnostic accuracy of sonohysterography, transvagi­nal sonography, and hysterosalpingography in patients with uterine cavity diseases. Fertil Steril. 2000;73(2): 406–11.
28. Makris N, Skartados N, Kalmantis K, Mantzaris G, Papadimitriou A, Antsaklis A. Evaluation of abnor­mal uterine bleeding by transvaginal 3-D hystero­sonography and diagnostic hysteroscopy. Eur J Gynaecol Oncol. 2007;28(1):39–42.
29. Yucebilgin MS, Aktan E, Bozkurt K, Kazandi M, Akercan F, Mgoyi L, Terek MC. Comparison of hydrosonography and diagnostic hysteroscopy in the evaluation of infertile patients. Clin Exp Obstet Gynecol. 2004;31(1):56–8.
30. Alborzi S, Dehbashi S, Khodaee R. Son­ohysterosalpingographic screening for infertile patients. Int J Gynaecol Obstet. 2003;82(1):57–62.
31. Bacelar AC, Wilcock D, Powell M, Worthington BS. The value of MRI in the assessment of traumatic intra-uterine adhesions (Asherman’s syndrome). Clin Radiol. 1995;50(2):80–3. Thomson AJ, Abbott JA, Deans R, Kingston A,
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34. Magos A. Hysteroscopic treatment of Asherman’s syndrome. Reprod Biomed Online. 2002;4 Suppl 3:46–51.
35. Salat-Baroux J, Pambou O, Guyot B. Hysteroscopic cure under ultrasonic control of complex and/or recur­rent uterine synechiae. [Article in French]. Presse Med. 1995;24(17):811–4.
36. Heinonen PK. Intrauterine adhesions – Asherman’s syndrome. [Article in Finnish]. Duodecim. 2010; 126(21):2486–91.
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38. Bettocchi S, Achilarre MT, Ceci O, Luigi S. Fertility­enhancing hysteroscopic surgery. Semin Reprod Med. 2011;29(2):75–82.
39. Shushan A, Protopapas A, Hart R, Magos AL. Diagnostic and therapeutic advantages of hystero­scopic surgery in management of intrauterine lesions in postmenopausal women. J Am Assoc Gynecol Laparosc. 2001;8(1):87–91.
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41. Pace S, Stentella P, Catania R, Palazzetti PL, Frega A. Endoscopic treatment of intrauterine adhesions. Clin Exp Obstet Gynecol. 2003;30(1):26–8.
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44. Capella-Allouc S, Morsad F, Rongières-Bertrand C, Taylor S, Fernandez H. Hysteroscopic treatment of severe Asherman’s syndrome and subsequent fertility. Hum Reprod. 1999;14(5):1230–3.
45. Shokeir TA, Fawzy M, Tatongy M. The nature of intrauterine adhesions following reproductive hys­teroscopic surgery as determined by early and late follow-up hysteroscopy: clinical implications. Arch Gynecol Obstet. 2008;277(5):423–7.
46. Yasmin H, Nasir A, Noorani KJ. Hysteroscopic man­agement of Ashermans syndrome. J Pak Med Assoc. 2007;57(11):553–5.
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Sonohysterography in Reproductive Medicine

Ilan Tur-Kaspa and Laurel A. Stadtmauer
1 3

Introduction

The existing practice guidelines, indications, and contraindications and the optimal technique for Sonohysterography (SHG) are reviewed. This will include a discussion on how to make the pro­cedure pain free for women by using fl exible catheters and gentle movements, infl ating the balloon inside the cervix rather than inside the uterine cavity, and injecting the saline slowly. The main focus will be on diagnosis of intrauter­ine abnormalities through SHG rather than their treatment thereafter. We conclude that SHG is a safe, accurate, cost-effective, and easy-to­perform procedure, for patients as well as for physicians, to evaluate intrauterine pathology and can be used as the primary diagnostic tool for the evaluation of infertility and before ART.
I. Tur-Kaspa , MD (*) Institute for Human Reproduction (IHR), Department of Obstetrics and Gynecology , The University of Chicago , 409 W. Huron St. , Chicago , IL 60654 , USA e-mail: drtk@infertilityihr.com
L. A. Stadtmauer , MD, PhD Department of Obstetrics and Gynecology , Eastern Virginia Medical School, Jones Institute for Reproductive Medicine , 601 Colley Avenue , Norfolk , VA 23507 , USA e-mail: stadtmla@evms.edu

SHG vs. Hysteroscopy

Sonohysterography (SHG) was fi rst described in 1986 by Randolph et al. [ 1 ]. Randolph et al. instilled saline into the uterus to provide contrast during transabdominal US and compared the SHG fi ndings in 61 women to hysterosalpingog­raphy (HSG) and laparoscopy/hysteroscopy. They concluded that real-time US with fl uid installation provides an accurate alternative to HSG in screening for uterine abnormalities and tubal patency. Syrop and Sahakian were the fi rst to describe transvaginal SHG in 1992, followed by Parsons and Lense in 1993 [ 2 , 3 ].
For a long time hysteroscopy with direct visualization of the intrauterine cavity was con­sidered the gold standard for diagnosing uterine abnormalities [ cavitary abnormalities in women screened by SHG or hysteroscopy for infertility range from 11 to 45 %, with polyps range between 6 and 25 % [
5 , 14 ]. In the last 15 years, accumulating
evidence-based data, including randomized con­trol trials, systematic reviews, and meta-analyses, has demonstrated that SHG has comparable sen­sitivity, specifi city, and accuracy in diagnosing intrauterine abnormalities as hysteroscopy [ 7 – 13 ,
15 – 21 ]. Therefore, SHG and other ultrasonog-
raphy techniques may be used as effectively as hysteroscopy for diagnosing intracavitary abnor­malities [ 8 , 10 , 11 ]. Pre-IVF SHG was shown to be effective at limiting cycle cancellations caused by endometrial polyps [ be highly valuable as the fi rst line of offi ce-based
4 – 13 ]. The percentage of intra-
22 ], and it was shown to
L.A. Stadtmauer, I. Tur-Kaspa (eds.), Ultrasound Imaging in Reproductive Medicine, DOI 10.1007/978-1-4614-9182-8_13, © Springer Science+Business Media New York 2014
167
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I. Tur-Kaspa and L.A. Stadtmauer
diagnostic tool for patients with recurrent IVF implantation failure [ 23 ]. These data may explain why most of the high- performing IVF programs in the US use SHG for the evaluation of uterine cavity before ART [ 24 ].
In addition, cost analysis comparing SHG vs. hysteroscopy screening prior to IVF showed that using SHG is more cost-effective. While hystero­scopic screening is cost-effective [ 25 ], Kim and Rone [ 26 ] have shown that SHG is more cost- effective than hysteroscopy. They calculated the average cost per patient ( n = 229) of SHG screening and hysteroscopy in the subset of patients who had signifi cant and/or correctable abnormalities ( n = 35,
15.3 %). The cost per patient using SHG screening with additional hysteroscopy as needed was $645. If hysteroscopy would have been used to screen the same group of patients instead of SHG, the cost per patient would have been $1281.

Practice Guidelines for SHG

The American Institute of Ultrasound in Medicine (AIUM) has published in March 2008 [ 27 ] a prac- tice guideline for ultrasonography in reproductive medicine. In the same year, the American College of Obstetrics and Gynecology (ACOG) published a technology assessment on SHG, in collaboration with AIUM; the Society for Reproductive Endocrinology and Infertility (SREI), an affi liate of the American Society for Reproductive Medicine (ASRM); and the American College of Radiology (updated in 2012) [ 28 ]. The reader is highly encour- aged to review these guidelines. They describe the technique, the indications and contraindications, and the qualifi cations and responsibilities of the physician performing the SHG. The authors of this chapter have found it easy to adhere and to comply with the above guidelines in their practices and have incorporated them into this review.

Indication and Contraindication

The AIUM and ACOG guidelines [ 27 , 28 ] describe the indications and contraindications for SHG. The most common indication for SHG is pre- and
postmenopausal abnormal uterine bleeding [ 29 , 30 ]. Screening of the uterine cavity prior to ART and for the evaluation of infertility and habitual abortions is the second most common indication. SHG may be performed for the evaluation of con­genital or acquired (fi broids, polyps, and syn­echiae) uterine anomalies and preoperative and postoperative evaluations of the uterine cavities. SHG may also be performed for further diagnosis of any suboptimal imaging of the endometrium and when focal or diffuse endometrial thickening or abnormalities are seen on a regular TVUS.
The two main contraindications for SHG is pregnancy and pelvic infection or unexplained pelvic tenderness. Abnormal uterine bleeding (AUB) is not a contraindication, though it may make the interpretation of the fi ndings more chal­lenging [ 20 ]. Tur-Kaspa et al. [ 14 ] have prospec- tively analyzed SHG of 409 consecutive patients with AUB and have found 37.2 % of intracavitary abnormalities, mainly polyps and submucosal fi broids. Goldstein [ 30 ] has suggested “ultrasound fi rst” as an approach to women with postmeno­pausal bleeding. SHG may be used for triage by identifying patients with no disease vs. those with focal or global abnormalities. Furthermore, patient acceptability and diagnostic capability of SHG is high, and it reduces demand for hysteros­copy [ 29 ]. SHG- guided endometrial biopsy pro- vided an accurate pathological diagnosis in 89 % of patients compared to 52 % with blind endome­trial sampling [ 29 , 31 ].

SHG Procedure [ 14 , 27 , 28 , 32 ]

Menstrual dating should be documented and pregnancy should be ruled out before performing SHG. The best timing for performing SHG is after the menstrual fl ow and prior to ovulation, in cycle days 5–10. This is when the endometrial lining is most symmetrical and precludes the chance for an early pregnancy. During the luteal phase, the lining is thickened and more echo­genic and may be associated with a higher false­positive rate of polyps. Using birth control pills may assist in scheduling this test at any day of the menstrual cycle.
13 Sonohysterography in Reproductive Medicine
169
Patients should be informed of alternative procedures and the possible risks and complica­tions of SHG (mainly discomfort, low risk of infection, and bleeding) and then sign a consent form. Pretreatment antibiotic is not recom­mended routinely unless the patient has a history of gynecological infections or tubal factor infer­tility [ 33 ]. Several RCTs, using different analge- sics, have failed to demonstrate benefi ts of using any drug to signifi cantly reduce pain during or after SHG [ 34 – 36 ]. Unless indicated, no analge- sics or sedatives are routinely needed before, dur­ing, or after SHG, since it may be considered as a pain-free procedure [ 14 , 37 ].
Prior to SHG, TVUS is performed with rou­tine evaluation and measurement of the uterus, endometrium, and ovaries. The presence of fl uid in the cul-de-sac should be noted, and any pelvic abnormal fi ndings such as hydrosalpinges should be documented. If a patient had a baseline TVUS on day 3 of her period and returns for SHG a few days later, then a quick scan for the evaluation of the uterine cavity and of fl uid in the cul-de-sac may be performed after the insertion of the cath­eter before the injection of the saline.
A speculum is placed in the vagina to visualize the cervix. After cleansing the external os with betadine or equivalent solution, the SHG catheter is inserted into the cervical canal. The SHG cath­eter should be prefi lled with saline in order to avoid infusing air bubbles into the uterine cavity. There are many catheter options, including HSG/ SHG curved catheters, intrauterine insemination catheters, and balloon SHG/HSG catheters. Any rigid catheter, which requires grasping the cervix with a tenaculum, may induce signifi cant pain for the patient. If a balloon catheter is used, it is pre­ferred to infl ate the balloon intracervically rather than intrauterine, and the appropriate position of the catheter may be confi rmed by pulling it slightly. An RCT recently showed a signifi cantly less fl uid used for SHG and signifi cantly less pain felt by patients when the balloon was infl ated inside the cervix rather than in the lower uterine segment [ 38 ]. Furthermore, by infl ating the bal- loon intracervically, one may avoid balloon hyperinfl ation inside the uterine cavity, which may displace and obscure a pathological fi nding,
such as endometrial polyp. Next, the speculum is removed and the TVUS probe is inserted into the vagina. Physiological saline solution is then slowly injected to distend the endometrial lumen under direct real-time visualization. Injecting the fl uid slowly is mandatory to avoid abrupt uterine distension and pain. Documentation should include images of the endometrial cavity, includ­ing the lower segment and the upper cervical canal in at least two planes, longitudinal and transverse (Fig. 13.1 ). The reader is encouraged to read the offi cial guidelines set by ACOG and AIUM [ 27 , 28 ].

SHG for Congenital Uterine Anomalies

SHG is a cost-effective method available in an outpatient setting which is highly accurate in identifying uterine anomalies, especially septate and bicornuate uterus [ 44 ]. Mullerian anomalies are congenital defects in the development of the uterus and the upper vagina. The ability of 2D US to distinguish between different types of uterine anomalies is limited and operator depen­dent. The fi nding of a uterine anomaly may affect the management of the infertile and/or pregnant woman and the pregnancy outcome. In a recent meta-analysis [ 39 ], including 94 obser- vational studies comprising 89,861 women, the prevalence of uterine anomalies diagnosed by optimal tests was 5.5 % (95 % CI, 3.5–8.5) in unselected population, 8.0 % (95% CI, 5.3–12) in infertile women, 13.3 % (95 % CI, 8.9–20.0) in women with a history of miscarriage, and
24.5 % (95 % CI, 18.3–32.8) in women with miscarriage and infertility.
Congenital uterine anomalies are associated with poor reproductive outcome [ 40 ]. All uterine anomalies are associated with an increase inci­dence of fetal malpresentations at delivery. Unifi cation defects do not reduce fertility but some defect, in particular bicornuate uteri, are associated with aberrant outcomes throughout the course of pregnancy. Canalization defects appear to reduce the chance of clinical pregnancy and to increase risk of preterm delivery. These are more
170
Fig. 13.1 2D longitudinal ( upper image ) and transverse ( lower image ) images of the uterus showing adequate distention of the endometrial canal with saline during SHG
I. Tur-Kaspa and L.A. Stadtmauer
profound in cases of septate uteri. Arcuate uteri, while previously considered to have no reproduc­tive sequelae, are specifi cally associated with poor outcomes in late pregnancy, i.e., second-tri­mester miscarriage and malpresentation [ 40 ].
Uterine anomalies are defi ned by the cri­teria outlined by the American Society of Reproductive Medicine [ 41 ]. The visualiza- tion of the uterine fundus at the coronal plane is necessary for classifying uterine shape. SHG has been shown to have superior diagnostic abil­ity with compared with HSG and 2D US for the evaluation of uterine malformation. Tur-Kaspa
et al. [ 14 ] studied prospectively the prevalence of uterine anomalies diagnosed by SHG in 600 consecutive infertile patients compared to 409 patients with AUB. While the prevalence of septate uterus was 3 % in each group, arcuate uterus was signifi cantly more common among the infertile patients (15 % vs. 6 %, respec­tively). All other anomalies had <1 % frequency in either group. Tur-Kaspa et al. [ 14 ], as well as others [ 7 – 11 ], concluded that SHG is an excel- lent method for the evaluation of congenital uter­ine anomalies. 3D SHG may be needed in some cases to assist in the fi nal diagnosis.
13 Sonohysterography in Reproductive Medicine
Fig. 13.2 2D longitudinal image of SHG demonstrating intrauterine adhesion at the lower uterine segment, connecting the anterior and the posterior walls of the uterus
Fig. 13.3 2D longitudinal image of SHG demonstrating two polyps protruding into the uterine cavity
171

SHG for Acquired Uterine Abnormalities

SHG can serve as a fi rst-line test for the evalua­tion of acquired intrauterine abnormalities such as adhesions (Fig. 13.2 ), polyps (Fig. 13.3 ), and fi broids. Tur-Kaspa et al. [ 14 ] have documented that intracavitary abnormalities are signifi cantly more frequent among patients with AUB than with infertility. Polyps were the most common
abnormal fi nding among patients with AUB or infertile women (30 and 13 %, respectively) [ 14 ].
Submucosal fi broids were found in 9 % of the AUB group and 3 % among infertile women [ 14 ]. Submucosal fi broids have been shown by meta­analysis to signifi cantly lower pregnancy rates in ART and should be removed by operative hyster­oscopy [ 4 , 6 ]. Besides infertility, the submucosal fi broids may cause bleeding and miscarriages. The European Society of Hysteroscopy has developed
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I. Tur-Kaspa and L.A. Stadtmauer
Fig. 13.4 3D SHG images of a uterine polyp. They are able to show the size and location of the stalk of the polyp more accurately in preparation for operative hysteroscopy and for consulting the patient
a classifi cation system for fi broids which can also assist in the surgical approach. A Type 0 submu­cosal fi broid has no myometrial invasion, while a T1 has <50 % extension and T2 has more than 50 % extension into the myometrium. The TO and T1 are appropriate for the hysteroscopic approach, while the T2 may require more than one procedure or be removed laparoscopically.
the evaluation of postmenopausal bleeding, 2D and 3D SHG have similar diagnostic accuracy as hysteroscopy with higher patient acceptabil­ity of SHG [ 45 , 46 ].
A 3D US, in comparison to a 2D US, allows for the visualization of the entire uterine cavity in the coronal view; it can detect the exact place­ment of uterine fi broids, polyps, and synechiae in the cavity, as well as the mean diameter of differ­ent tissues. A 3D US examination comprises

2D vs. 3D SHG

approximately four steps: (1) data acquisition, (2) volume calculation, (3) image animation, and (4)
When the option of having a 3D SHG scan is available, it may shorten the procedure and the volume of the saline used [ 42 ]. 3D SHG vs. 2D SHG is more accurate for diagnosing congeni­tal uterine anomalies. For acquired uterine anomalies, in experienced hands, 3D will not improve the accuracy, but may assist it for bet­ter imaging (Figs. 13.4 and 13.5 ) [ 43 , 44 ]. For
data storage and transfer. The scans can be obtained either by freehand, by manual move­ment through the region of interest (ROI), or, automatically, by sweeping through the ROI. 3D US needs post-processing of the received data. Data can be stored and visualized in various displays such as multiplanar with navigation through the planes or surface rendering mode.
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Fig. 13.5 3D SHG image of a corneal uterine polyp pro­viding excellent information for the practitioner and patient on the size and location of the polyp
For more details on 3D US technique, the reader may refer to Chap. 2 .
A saline infusion enhances the contrast in a 3D US and can facilitate the accurate diagnosis of congenital uterine anomalies, especially the arcuate uterus (Fig. 13.6 ) compared with the septate uterus (Fig. 13.7 ) and the bicornuate uterus. The serosal edge and the fundal indenta­tion can be clearly seen. Through TUI tomo­graphic imaging, a series of images can visualize the leiomyomata protruding into the uterine cavity vs. deviating the endometrial cavity.
3D adds value to 2D SHG by improving with visualization of the uterine fundus [ 47 ]. Others suggest that when the SHG is performed by an experienced examiner, 3D does not add additional value to the 2D SHG [ 48 ]. It is the opinion of the authors that adding a 3D US to a 2D SHG will allow the exam to be completed faster with the same or better accuracy. Still in most cases, 2D SHG is adequate for diagnos­ing abnormal intracavitary fi nding.
Fig. 13.6 3D SHG demonstrating an arcuate uterus. The visualization of the fundal area at the coronal plane and the ability to measure the depth of the anomaly can easily defi ne arcuate uterus and rule out a septum