INTRODUCTION

Ultrasound within the field of gynecology has played an imperative role in the diagnosis of various conditions. Real time ultrasonography provides a useful adjunct to many minor gynecological procedures, including oocyte collection and embryo transfer in assisted reproductive technology (ART), aspiration of ovarian cysts or pelvic abscesses, insertion and removal of intrauterine devices and guiding endometrial biopsies. As such, advancement in technology of this non-invasive and cost-effective resource has enabled wider application of the modality across the speciality, with many gynecologists now skilled in carrying out the above procedures through office based ultrasound. However, the use of intraoperative ultrasound (IOUS) is not as widely reported in gynecological surgery, despite it being considerably implemented across other surgical specialties.

Intraoperative ultrasound

IOUS was first pioneered by a general surgeon in 1979, whereby the diagnosis of biliary calculi was confirmed during cholecystectomy.¹ It was particularly effective in the resection of hepatocellular carcinoma associated with cirrhosis, whereby lesions <5 cm identified during pre-assessment were missed intraoperatively in 50% of patients, due to the lesions being too small to be identified, or not palpable intraoperatively.² Given that tumors as small as 3–5 mm can be detected by IOUS, the diagnostic modality is deemed to be more accurate at diagnosing metastasis when compared to computerized tomography (CT), percutaneous ultrasound and surgical exploration, with a sensitivity and specificity reported as more than 90% as an effective screening test.^3,4,5 Furthermore, in 5–10% of surgeries performed during colorectal cancer surgery, IOUS identified new occult liver metastatic lesions.^4,5,6 The ability for IOUS to determine the margins of cryosurgical ablation has further revolutionized the treatment of tumor deposits deemed previously unresectable.⁷ Consequently, approximately 30–50% of operations performed for the surgical management of hepatic tumors have been altered as a result of IOUS.^8,9,10,11 In the 1980s, IOUS was also introduced during neurosurgery, with evidence suggesting that utilization of the tool depicted more accurate localization and characterization of intracranial masses.¹² It has since also been used to resect pancreatic cancers, thyroid tumors and within breast surgery.¹³

Despite the vast array of evidence and applicability of IOUS in other surgical specialties, the implementation of this technique remains in its infancy, particularly with regards to complex gynecological surgery. In a recent systematic review of 45 studies where IOUS was utilized in gynecological surgery, it was predominantly in the context of operative hysteroscopic or laparoscopic surgery, using the following ultrasound (US) modalities: transabdominal US (TAUS), transvaginal US (TVUS), laparoscopic US (LUS), transrectal US (TRUS) or contact US (CUS) during open surgery.¹⁴ We describe herein the application of IOUS used in gynecological procedures thus far.

Laparoscopic myomectomy

The use of IOUS for laparoscopic myomectomy was first described in 2004.¹⁵ As it was not feasible at the time of laparoscopy to palpate the myoma for resection, a sterile laparoscopic ultrasound transducer was introduced through the 10–12 mm trocar, with an adjustable head allowing for 90 degree movement in four directions to maximize tissue contact. The US transducer allowed for localization of the myoma to determine the incision site for hysterotomy, in the absence of serosal distortion visible to the naked eye, thus minimizing healthy tissue injury.¹⁵

Since then, there has been significant evidence to suggest that the use of IOUS is safe and effective in the management of leiomyomas and fibroids.^16,17,18,19 In particular, IOUS can facilitate the screening and laparoscopic resection of deep intramural myomas within the myometrium through either TVUS or endoscopic probes, potentially avoiding a laparotomy. It also improves surgical technique by accurately assessing the number, location and dimension of the fibroids, negating the requirement for expensive pre-operative imaging.

In regards to open myomectomies, IOUS has also demonstrated superior outcomes, with lower rates of residual myomas observed postoperatively, thus less risk of recurrence requiring further surgery, when compared to without IOUS.²² Furthermore, submucosal myomas with an intramural component of more than 50% are associated with increased risk of intraoperative complications during hysteroscopic resection, necessitating the requirement for open surgery.²³ Through the use of IOUS, however, it may be feasible to use laparoscopy to treat fibroids classified as Munro types 2, 3 and 4,²⁴ particularly when conventional laparoscopy may be associated with an endometrial defect following enucleation of the myoma.

Hysteroscopy and transcervical surgery

Operative hysteroscopy is often used for the resection of endometrial polyps, leiomyomata, adhesions and septoplasty. The introduction of IOUS has been successfully demonstrated during hysteroscopic resection of metroplasty of a uterine septum, whereby complete resection was reported in 100% of the cases operated on, and assessment during follow up identified a regular endometrial cavity.^25,26,27 Absence of ultrasound guidance was associated with an increased rate of uterine perforation.²⁸ In women of reproductive age, IOUS used during the resection of intrauterine septum was also associated with favorable reproductive outcomes. This was demonstrated by a study of 34 patients presenting with primary subfertility secondary to the pathology, whereby 14 spontaneous conceptions resulting in 13 livebirths following the procedure were achieved.²⁹ Various studies have also since described outcomes on the use of IOUS during hysteroscopic resection of fibroids and reported complete excision of the tissue in all cases performed.^30,31

Ultrasound guidance is also effective during instrumentation of the uterus in cases of Asherman’s syndrome, where intrauterine adhesions significantly reduce visualization of the cavity, thereby reducing the risk of uterine perforation.³² An abdominal ultrasound transducer can be used intraoperatively in the presence of a full bladder, to guide the surgeon during dilation, in cases of a tortuous or stenosed cervix, aiding the surgeon to manipulate hysteroscopic instruments.

IOUS with TAUS, TVUS or TRUS during transcervical surgery has also been observed in the surgical management of cornual ectopic pregnancies.^33,34 In one particular case of IOUS used to guide complete resection of a cervical ectopic in a heterotopic pregnancy, the intrauterine pregnancy was preserved, which subsequently resulted in a livebirth at term.³⁵

Reproductive surgical procedures

Within ART, the implementation of ultrasound guided embryo transfer has significantly increased implantation and clinical pregnancy rates, when compared to the clinical touch blind method performed in the absence of US.^36,37 Moreover, dilation and curettage procedures performed with continuous ultrasound guidance are associated with a significantly lower complication rate (RR 0.23, CI 0.08–0.67), including reduced intraoperative blood loss, procedure time, analgesic requirement, post-operative bleeding and infection rates.³⁸

Vaginal surgery

IOUS has been effectively used during vaginal pelvic surgery using TAUS or TVUS in a study of 29 patients to aid posterior culdotomy, whilst improving access to the pouch of Douglas.³⁹ No complications were reported amongst the cohort, contrary to the 162 patients who had the procedure in the absence of ultrasound guidance and experienced six complications, including three rectal injuries, one ureteric and two retroperitoneal fluid collections.³⁹

Fertility sparing surgery

The use of IOUS has also been described in the context of fertility sparing surgery (FSS); the aim of which is to resect gynecological pathology, whilst preserving reproductive potential and ability to conceive. In the management of borderline ovarian tumors (BOTs) for example, conventional methods to treat primary or recurrence of disease have included performing an oophorectomy to ensure complete resection of pathology. Through surveillance monitoring with ultrasound, it is possible to identify recurrences presenting as small intraovarian deposits, too small to be visualized at laparoscopy (Figures 1 and 2).⁴⁰ Although it is feasible to manage such patients conservatively and operate only once the lesion is large enough to be seen at laparoscopy,⁴¹ it is possible that delaying intervention may later cause upstaging of disease, subjecting women to unnecessary invasive surgery. Recurrent serous BOTs (sBOTs) also increase in size at a rate of approximately 0.06 mm per month, and therefore, the time it takes for the lesion to be deemed adequate enough to perform laparoscopic resection, may delay the women’s future plans for pregnancy.⁴¹ IOUS using TVUS and TRUS modalities have been successfully used to treat a series of seven women presenting with a first recurrence of sBOTs, who wished to preserve their fertility.⁴⁰ The women in the series all underwent ultrasound guided ovarian wedge resection (UGOWR) of lesions between 12 and 37 mm and deeply embedded within ovarian tissue to be seen laparoscopically.⁴⁰ Six of the seven women operated on did not develop recurrence of disease during a follow up time of 1–20 months, thus demonstrating safe and complete resection of non-benign intra ovarian lesions is feasible.⁴⁰ UGOWR has since been used in the management of primary BOT, with again no reported recurrence of disease identified on follow up, particularly in cases where the procedure was not performed in combination with other methods of FSS.⁴² Recurrence of BOT has also been successfully resected using LUS.⁴³ The advantages of using LUS over TVUS or TRUS in the case reported, were described as closer proximity of the probe to the lesion, thereby reducing abdominal or vaginal wall inference and risk of infection, whilst also not having to change the laparoscopic position of the patient.⁴³

Intraoperative LUS has also been used to perform FSS for the treatment of Herlyn-Werner-Wunderlich syndrome, whereby direct contact of the LUS probe with the uterus provided enhanced visualization of the origin of a longitudinal vaginal septum, which the surgeon was then able to excise through a transvaginal approach. Thus, the use of LUS in this case, was imperative in both the diagnosis and treatment of a complex uterine malformation, with excellent surgical outcomes reported.⁴⁴

Open gynecological surgeries

Further use of IOUS in FSS includes a case report on the application of CUS during open surgery to resect a placental site trophoblastic tumor in a patient wishing to preserve her fertility. The use of IOUS enabled accurate hysterotomy, minimizing the excision of healthy tissue whilst preserving the woman’s fertility, thus avoiding the need for hysterectomy which would render the woman infertile. The patient subsequently went on to conceive naturally and delivered a baby at term.⁴⁵

IOUS in open surgery has also been performed in a woman at 14 weeks' gestation who presented with abdominal pain, secondary to a fundal intramural subserous myoma measuring 157 × 90 mm, as well as other smaller myomas diagnosed, causing compression of the gestational sac. A convex transducer placed directly onto the uterine serosa intraoperatively, guided the surgeon in regards to location of the myoma, its relationship with the endometrial cavity and the optimal site for incision, whilst also providing information on fetal viability.⁴⁶

Radical debulking surgery

IOUS can be used in complex gynecological procedures for diagnostic purposes, particularly when suspicious lesions are identified on palpation during open surgery. This was observed in a woman who underwent bilateral adnexectomy, hysterectomy, omentectomy and peritoneal biopsies for bilateral sBOT.⁴⁷ During which, the lumbar-aortic region appeared enlarged on palpation, and thought to be a lymph node. IOUS assessment of the lesion identified a hypoechoic lymph node in the precaval region measuring 9.6 mm, with an irregular echo structure, no color Doppler flow and presence of calcification.⁴⁷ The lymph node was subsequently isolated and excised surgically based on the US findings, and identified as adenocarcinoma on frozen section analysis. As such, the surgical procedure was altered by then including para-aortic and bilateral iliac lymphadenectomies.⁴⁷ Histology confirmed the lymph node was a metastasis of low grade serous carcinoma, which could have been missed in the absence of the information provided from the IOUS.⁴⁷ A similar case has been reported whereby two enlarged cardiophrenic lymph nodes were effectively resected during primary debulking surgery for advanced ovarian cancer, that was only identified by IOUS following initial abdominal cytoreduction.⁴⁸

Improved visualization of pelvic anatomy

IOUS can also be used during laparoscopic surgery to identify pelvic anatomy and avoid tissue injury to adjacent structures. This has been demonstrated in a case where cystic adenomyosis using TVUS with LUS guidance was safely resected, consequently resolving symptoms of severe dysmenorrhoea.^49,50 Furthermore, TAUS during laparoscopy has helped retrieve a lost intrauterine device (IUD) identified in the abdominal cavity during preoperative imaging, but not seen laparoscopically.⁵¹ Use of the IOUS confirmed the presence of a tubular hyperechoic structure in the abdominal cavity, precisely localizing the IUD within the bowel loops, thus avoiding the conversion to laparotomy to retrieve the device.⁵¹

IOUS also provides excellent diagnostic accuracy when characterizing adnexal masses. In one study of 58 women, the accuracy of characterizing ovarian cysts was significantly higher following laparoscopic ultrasonography than preoperative TVUS (83.8% vs. 73.5% respectively, p < 0.05), when compared with histological diagnosis.⁵² Accuracy in diagnosis was particularly significant in the cases of diagnosing endometriomas or dermoid cysts from other benign pathology.⁵²

EVIDENCE BASED PRACTICE

Indications for the use of IOUS

The primary indications for the use of IOUS include: (1) to acquire new information not otherwise available; (2) to complement or replace intraoperative radiography; (3) to confirm completion of the operation; and (4) to guide surgical procedures.

IOUS provides real-time imaging and intraoperative exploration, not previously available during pre-operative assessment. This aims to accurately reassess the location of previously diagnosed lesions, exclude previously suspected pathology, assess for new lesions, establish the anatomic structures surrounding the pathology such as blood vessels, before performing tissue dissection/resection to ensure optimization of the surgical approach and minimize intraoperative complications. Given the improved diagnostic accuracy of IOUS, it also has the potential to negate the requirement for the use of contrast during preoperative imaging assessment. It provides a useful tool for assessing complete excision of lesions, preventing the requirement for further surgery. IOUS also guides procedures requiring surgical tissue dissection or intervention, such as needle or cannula insertion during the aspiration of pelvic cysts or abscesses, or during probe placement.

For the purpose of this chapter, we describe the application of IOUS performed either transabdominally during hysteroscopic or transcervical (without hysteroscopic guidance) surgery and transvaginal or transrectal insertion during laparoscopic surgery.

Indications for the use of IOUS during operative hysteroscopy include the resection of intra-uterine pathology, such as complete or partial uterine septum, submucous or intramural fibroids, uterine synechiae or Asherman’s syndrome, atypical placental site nodules, osseous metaplasia of the endometrium and for the surgical management of miscarriage (Table 1). Indications for transcervical surgery without hysteroscopy, include dilating a stenosed cervical canal after conization or trachelectomy or the treatment of cervical or cornual ectopic pregnancies. IOUS in this context aims to reduce the risks of uterine perforation or incomplete resection of the lesion.

The indications for IOUS during operative laparoscopic surgery include resection of pelvic lesions not visualized laparoscopically, such as small BOTs and ovarian cysts, or when pelvic adhesions obscure visualization of the ovaries (Table 1). During extensive adhesiolysis of the pelvic side walls, the US can improve access to the lesion and minimize risk of injury to the ureter or pelvic vasculature. When treatment of ovarian pathology is required, IOUS should also be used to delineate diseased pathology from healthy ovarian tissue, particularly in women of reproductive age, in order to optimize preservation of fertility where possible. The advantages and disadvantages of IOUS are listed in (Table 2).

Contraindications

A well-known complication associated with the utilization of distention media during gynecological procedures, for example, during hysteroscopic surgery, is fluid overload, with or without electrolyte imbalance.⁵³ The incidence of which is reportedly less than 5% secondary to operative hysteroscopy.⁵⁴ Despite the risks of systemic absorption of isotonic saline distension fluid, through retrograde passage of fluid through the fallopian tubes, endometrium, or via vasculature and sinuses open during resection of uterine tissue, especially when the intrauterine pressure is greater than the pressure in the venous sinus or blood vessels,⁵³ there have been no reported incidences of fluid overload following the use of intraoperative ultrasound during laparoscopic surgery. This is unsurprising given that a fluid deficit of 2500 ml is the threshold required to define fluid overload when using isotonic solutions, and more than 1000 ml when using hypotonic solutions in women of reproductive age.⁵⁵ Given that only 500 ml of isotonic saline is required as a distention media during IOUS laparoscopic surgery, it is therefore unlikely to result in this complication. In the context of hysteroscopic surgery, the use of intraoperative ultrasound does not impact the volume of fluid media required during operative surgery, therefore the <5% risk of fluid overload associated with operative hysteroscopic procedures remains the same.

Transabdominal ultrasound for hysteroscopic or transcervical (without hysteroscopic guidance) surgery

A curvilinear or phased array probe may be used. Both sagittal (longitudinal) and transverse views of the uterus should be obtained. TAUS is usually operated at lower frequencies of 3.5 MHz, allowing for deeper signal penetration, although with poorer resolution when compared to probes used for TVUS.⁵⁶ The patient is positioned in the dorsal lithotomy position. The preferred positioning of the sonographer is to stand at the right side of the patient, with the surgeon sitting between the legs of the patient. This allows for the sonographer to obtain adequate visualization of the cervix and uterus, whilst not confined to a space shared with the primary surgeon. TAUS allows for improved flexibility to image a larger field of view when compared to TVUS. The urinary bladder should be filled with 300 ml of saline solution to displace the uterus superiorly, for improved transabdominal views. During transcervical surgery, in the absence of hysteroscopy, the uterus is instilled with 30 ml of saline through the external os, to distend the uterine cavity and delineate anatomy from the pathology to be resected. The urinary bladder should be emptied at the end of the procedure.

Laparoscopic, transvaginal or transrectal ultrasound during laparoscopic surgery

IOUS for laparoscopy incorporates B-mode ultrasound with high frequency transducers. The higher frequency allows for greater resolution, despite penetrating less deeply. Most general surgeons use transducer frequencies between 7 and 8 MHz. This allows for the smallest of lesions to be detected, such as a 1 mm calculi, 2 mm cyst or a 3–5 mm tumor.² The use of color Doppler also allows for faster recognition of blood vessels from other pelvic structures.

The type of transducers used in IOUS have typically included linear, curvilinear (convex) and phased (sector) array. Linear 7.5 MHz probes in particular, are the preferred choice of transducer used in general surgery. In the context of IOUS within gynecology, it is important that the probe can be manipulated in small and narrow operating fields, thus high resolution endovaginal probes with three-dimensional (3D) imaging are frequently used, allowing detailed examination of pelvic anatomy. Laparoscopic probes are configured with linear or convex linear array transducers placed on the tip of a long shaft.⁵⁷ The shaft is <10 mm in diameter and 35–45 cm in length to allow a wide examination field from a single port. Such transducers are of 5–10 MHz frequency range.

The two techniques for scanning intraoperatively include contact and standoff. Contact scanning requires the probe to have direct contact with the organ/tissue surface to create a transcutaneous ultrasound effect. It allows for the examination of target lesions located deep within tissue (away from the probe). Standoff scanning, however, requires that the probe is positioned 1–2 cm away from the surface of the structure and immersed in saline.² It is particularly useful for the examination of the surface area of pelvic organs, or to examine superficial structures. As most gynecological procedures require examination of surface areas, the latter technique is predominantly used, with the ultrasound transducer inserted transvaginal or transrectal (in the case of when instrumentation of the uterus is required), to allow the surface of the pathology to remain immersed in saline, whilst maintaining an adequate distance from the probe.

IOUS in the management of surgical resection of ovarian or pelvic pathology

The patient is placed in the Trendelenburg or lithotomy position. Laparoscopic entry and peritoneal insufflation of carbon dioxide (CO₂) is performed to achieve a pneumoperitoneum. CO₂ has a hyperechoic effect on ultrasound which can cause suboptimal US views. Following laparoscopic entry and assessment of the operating field, 500 ml of normal saline (0.9%) is therefore infiltrated into the pelvis, for enhancement of the ultrasound image quality and transmission of the ultrasound, by acting as a conducting agent. This remains within the pelvis during the course of the operation. An assistant with competencies in pelvic ultrasound scanning inserts a probe with a sterile cover either transrectal or transvaginal, to provide real-time ultrasound images of the ovary, uterus, pelvic organs and pathology to be resected. As the probe is sterile, it can be used repeatedly throughout the operation. It is essential that IOUS is performed early in the operation to ensure newly diagnosed lesions can be identified, so that imaging can guide the surgeon, such that no residual pathology remains postoperatively. For this reason, the target organs are systematically scanned in the longitudinal and transverse view, with sliding, rotation and angulating of the probe encouraged. In the context of ovarian pathology, a non-traumatic instrument is then used to stabilize the ovary +/− pathology (e.g. ovarian cyst, BOT lesion within the ovary), whilst correlating between the laparoscopic and ultrasound images (Figure 3).

Diathermy can be used to demarcate the surface of the lesion on the ovary to be removed (Figure 4). The resection of ovarian pathology is then performed under continuous ultrasound guidance, above the level of the saline solution, ensuring the surgeon can differentiate between healthy ovarian tissue and ovarian pathology (Figure 5). It is imperative that communication between the sonographer and surgeon remains throughout the procedure, to co-ordinate the laparoscopic and ultrasound views. IOUS is then used to ensure that pathology has been excised completely (Figure 6 and 7) and the saline fluid is aspirated prior to closure of the abdomen following removal of the pathology through laparoscopic specimen retrieval bags, followed by routine laparoscopic closure of the abdomen (Videos 1 and 2).

Postoperative care

The postoperative management of patients undergoing IOUS does not differ from that of patients undergoing conventional operative hysteroscopy or laparoscopy. The patient can eat and drink after the operation and adequate analgesia should be administered. The patient is encouraged to mobilize and pass urine and may be able to go home the same day, depending on the complexity of the procedure performed.

FUTURE WORK

Future work will consist of developing ultrasound technology and instrumentation, and the incorporation of this intraoperatively. This will focus mainly on developing user friendly scanners and probes for surgeons, improved resolution and deeper sound penetration, harmonic imaging with contrast agents in the context of color Doppler imaging and refinement of 3D images to improve diagnostic accuracy.

Given that IOUS is deemed a low cost treatment and readily accessible, in addition to the fact that most training programs require trainees to achieve competencies in minimal access surgery and TVUS through objective structured assessment of technical skills,¹⁴ the use of IOUS is considered a proficiency that can be reproducible and implemented nationally, rather than a skill limited to specialist tertiary units. Training and education of IOUS therefore, should be encouraged and may be enhanced through the use of computer based US simulation.

Further high quality prospective studies assessing the efficacy of IOUS in gynecological surgery are also required, as opposed to reported experience and case reports only. As such, the authors of this chapter have designed a prospective two armed randomized controlled trial comparing laparoscopic ovarian cystectomy for the management of benign ovarian cysts, with ultrasound guided laparoscopic ovarian cystectomy (Trial Registration: NCT05032846).⁵⁸ The aim of the trial is to determine the efficacy of IOUS as an adjunct of FSS. The primary outcome will be to determine the difference in anti-Müllerian hormone (pmol/L) and antral follicle count measured at 3 and 6 months postoperatively, compared to the pre-operative baseline. Secondary outcomes will include assessment of various surgical and histopathological findings, such as duration of hospital stay (days), duration of surgery (minutes), presence of intraoperative cyst rupture (yes/no), presence of ovarian tissue within the resected specimen (yes/no) and the grade of follicles excised (0–4). The findings of this study will determine whether IOUS is able to optimize healthy ovarian tissue preservation during minimally invasive surgery for benign ovarian pathology. Conclusions will be disseminated to clinicians and used to provide informative counseling to patients to ensure they can make well-informed decisions regarding their future fertility, before deciding to undergo laparoscopic surgery for benign gynecological pathology.

SUMMARY

Evidence thus far suggests that the use of IOUS within gynecological surgery including operative hysteroscopy and laparoscopy for benign and pre-malignant conditions are associated with favorable surgical and reproductive outcomes. However, further high-quality studies are required, particularly to support the effectiveness of IOUS as an adjunct of fertility sparing surgery in women of reproductive age. The use of IOUS is considered a low cost and non-invasive tool, that can be widely implemented by all gynecologists who are skilled in ultrasound scanning.

PRACTICE RECOMMENDATIONS

PERMISSION

Permission to reproduce video images has been granted by Mr Joseph Yazbek.