The diagnostic performance of ultrasound in the diagnosis of indeterminate adnexal masses based on the O-RADS US scoring system

Abstract

Background

One of the most frequent reasons for gynecologic imaging is adnexal masses. The aim of the study is to assess the diagnostic performance of ultrasonography in the identification of ambiguous adnexal masses using the O-RADS US scoring system.

Methods

This study included 108 cases and involved females with indeterminate adnexal masses, with any age group who were sent to the diagnostic ultrasonography department for evaluation of a worrisome adnexal mass lesion. We excluded patients who refused the examination despite informed discussion with the sonographer and patients with a previous history of operated adnexal lesion.

Results

Based on the O-RADS US score, more than half masses (52.8%) were diagnosed as O-RADS 3, which is low-risk malignant, and 47.2% were diagnosed as O-RADS 4, being intermediate-risk malignant. Regarding US O-RADS categorization in relation to the reference results by pathology, 57 lesions were categorized as O-RADS 3 by the US, and 18 of them was diagnosed as malignant according to pathology. Out of 51 lesions categorized as O-RADS 4 by the US, 30 were diagnosed as benign by pathology. At cutoff 4, the O-RADS US score for malignancy gave a sensitivity of 93.13% (95% CI 25.13–80.78), specificity of 66.72% (95% CI 34.49–76.81), PPV of 93.18% (95% CI 26.07–58.16), and NPV of 75.42% (95% CI 52.13–81.17) with an overall accuracy of 92.56% (95% CI 38.10–72.06).

Conclusions

In order to distinguish between benign and malignant neoplastic lesions, the US O-RADS classification system is a crucial non-invasive diagnostic tool for suspected ovarian tumors.

Background

Adnexal masses are frequent, which leads to a heavy clinical workload for pathology, surgery, and diagnostic imaging. The majority of adnexal masses are benign and ultrasonography can reliably classify the majority of masses as benign or malignant [1].

However, even after ultrasonography utilizing simple rules or other ultrasonography grading systems, the diagnosis of 18–31% of adnexal masses remains uncertain [2].

Due to the possibility of upstaging a contained early-stage ovarian cancer or the risk of sample mistake leading to a missed cancer diagnosis, percutaneous biopsy of a suspected adnexal tumor is not recommended. Since only 8–20% of adnexal masses on ultrasonography are malignant, many women with sonographically ambiguous but benign adnexal masses endure potentially lengthy surgical treatments that may be unnecessary [3].

Ultrasound is the most used imaging modality for assessing the uterus, fallopian tubes, and adnexa in females. Because of its widespread availability, lack of radiation and low cost, ultrasonography is now the gold standard for evaluating the female pelvis. When demonstrating gynecological anatomy or assessing physiological or pathological changes, ultrasound is typically the first and only imaging modality employed [4].

Ovarian ultrasound (US) is the gold standard imaging modality for detecting and characterizing ovarian tumors because of its ease of use and lack of invasiveness [5]. Results from US color Doppler may enhance morphological evaluation of ovarian cancer risk [6].

In 2020, the American College of Radiology (ACR) published a consensus article on the O-RADS classification, a technique for assessing the likelihood of malignancy in adnexal tumors. The O-RADS approach uses six criteria to assess the potential danger posed by adnexal masses, adnexal masses with score 3 and 4 are considered indeterminate masses [7] (Table 1).

Table 1 O-RADS US scores [9]

The goal of the Ovarian-Adnexal Reporting and Data System (O-RADS) US risk stratification and management system is to standardize interpretations of US reports in order to reduce or eliminate ambiguity, thereby increasing the likelihood of accurately assigning the risk of malignancy to ovarian and other adnexal masses [8].

The purpose of this research was to evaluate the diagnostic performance of ultrasound using O-RADS US classification system in diagnosis of indeterminate adnexal masses.

Methods

Ethical consent

Academic and Ethical Committee approved the research (IRB Approval No. ZU-IRB#9240/12–1-2022). All participants agreed to participate in the research after signing an informed written permission form. The Declaration of Helsinki, a global standard for the ethical conduct of medical research involving human participants, has been followed throughout this project.

Population and study design

Between February 2022 and February 2023, this prospective study was conducted and included 108 patients with confidence interval 95%. We allocated patients from two hospitals who were sent to the diagnostic ultrasound unit, examined by a radiologist with 12-year experience in ultrasound and a radiologist with 5-year experience in ultrasound to evaluate a possible adnexal mass and Histopathologic diagnosis was the gold standard in patients managed by surgical treatment (57 lesions in our study). The other 39 lesions showed resolution and improvement on follow-up ultrasound or MRI scans.

• Inclusion criteria:

  • 1. age 16–65 years old.

  • 2. Female with sonographically indeterminate adnexal masses O-RADS US 3 & 4—according to the O-RADS US classification which was developed by an international multidisciplinary committee sponsored by the American College of Radiology-

ORADS US 3: low risk of malignancy (1 to < 10%)—needs a referral to ultrasound specialist or gynecologist with a view to MRI

• Unilocular > 10 cm (simple or non-simple) lesions looking like typical dermoids, endometriomas, or hemorrhagic cysts > 10 cm

• solid smooth lesion of any with color score 1

• multilocular cyst < 10 cm smooth inner wall with color score 1–3

O-RADS US 4: lesions with an intermediate risk of malignancy (10 to < 50%)—needs ultrasound specialist review or MRI as well as management by a gynecologist with gynecological oncology support or solely by a gynecological oncologist

• unilocular cyst with a solid component, any size, 1–3 papillary projections, any color score

• multilocular cyst with solid component, any size, color score 1–2

• multilocular cyst without solid component

  •  > 10 cm, smooth inner wall with color score 1–3

  • any size smooth inner wall with color score of 4

  • any size with an irregular inner wall or irregular septations of any color score

• solid smooth lesion of any with color score 2–3

Exclusion criteria:

• 1. The patients who refused the examination despite informed discussion with the sonographer

• 2. patient with a previous history of the operated adnexal lesion.

• 3. O-RADS US 1: physiologic category (normal premenopausal ovary)

  • ovarian follicle (< 3 cm)

  • corpus luteum (< 3 cm)

• 4. O-RADS US 2: almost certainly benign category (< 1% risk of malignancy)

  • simple cyst 3–5 cm

    • premenopausal: no follow-up

    • postmenopausal: 1-year follow-up

  • simple cyst 5–10 cm

    • premenopausal: 8–12-week follow-up

    • postmenopausal: 1-year follow-up

  • non-simple but unilocular cyst with smooth margins 3–10 cm

    • premenopausal: 8–12-week follow-up

    • postmenopausal: refer to ultrasound specialist or MRI; management by a gynecologist

  • non-simple but unilocular cyst with smooth margins < 3 cm

    • premenopausal: no follow-up

    • postmenopausal: 1-year follow up if referring to ultrasound specialist or MRI management by a gynecologist

  • lesions with "classical ultrasound characteristics" of the following but may have specific recommendations and measure < 10 cm:

    • typical hemorrhagic cyst

    • dermoid cyst

    • endometrioma

    • paraovarian cyst

    • peritoneal inclusion cyst

    • hydrosalpinx

• 5. O-RADS US 5: lesions with a high risk of malignancy (≥ 50%)—needs a referral to a gynecological oncologist

  • presence of ascites/peritoneal nodularity

  • unilocular cyst with 4 or more papillary projections

  • multilocular cyst with a solid component—color score 3–4

  • solid lesion—smooth outer contour, any size, color score 2–3

  • Solid irregular lesion of any size

U/S protocol and technique

All US tests were done using the same system (a SonoScape S40 Exp/S40 Pro/S40/S35 Digital Color Doppler ultrasound system) to rule out the probability of system-to-system variations in the ultrasound imaging, a trans-abdominal ultrasound was performed with a full bladder, or a trans-vaginal ultrasound was performed after UB evacuation. While the patient was lying supine, multidirectional sonograms were acquired using transducers with frequencies ranging from 2.5 to 8 MHz. Location, size, consistency, and clearly defined boundaries were used to classify each adnexal lesion. The vascularity of the lesion were evaluated using Power or color Doppler US, and to ensure the presence or absence of a solid component. Using the US O-RADS categorization system, we gave each lesion a score.

Reference standard

The US findings using the O-RADS classification system were correlated with surgical removal and pathology findings for suspicious masses, and the remaining O-RADS 3 ( low risk malignancy) lesions in young premenopausal patients were referred for MRI assessment before the final clinical diagnosis was made.

Statistical analysis

SPSS version 28 (IBM Co., Armonk, NY, USA) was used for the statistical analysis. The parameters' quantitative mean, standard deviation (SD), and range were given. The percentage and frequency distributions were used to depict the qualitative variables.

The diagnostic efficacy of several tests was compared using ROC curves with area under the curve (AUC) (where AUC > 50% represents acceptable performance and AUC 100% is the optimum performance for the test). To be statistically significant, the P value has to be less than 0.05 with two tails.

Results

This prospective study included 108 females with sonographically indeterminate adnexal masses, with ages ranging between 16 and 62 years (mean age of 42.92 ± 13.01 years). Most patients (91.7%) were married. Out of 108 patients, 61.1% were premenopausal, as shown in Table 2.

Table 2 Baseline characteristics and symptomatology of the studied patients (n = 108)

As shown in Table 2, all 108 patients suffered from pain, more than half patients (63.9%) suffered from constipation or diarrhea, 44.4% had fever, 41.7% had palpable mass or increased abdominal volume, 22.2% had vaginal bleeding, and 19.4% had urinary symptoms.

As regards the origin of the studied lesions, 99 were adnexal (out of which, 69 were ovarian, 21 were tubo-ovarian, and 9 were in broad ligament) and 9 were non adnexal (uterine lesions) as shown in Fig. 1.

Fig. 1

Origin of lesions detected in the studied patients

Over half of masses (52.8%) were classified as O-RADS 3 according to the O-RADS US stratification system which is low risk malignant as case in Fig. 2 and 47.2% were diagnosed as O-RADS 4 being intermediate risk malignant as case in Fig. 3, 4 and 5. Regarding US O-RADS classification in relation to the reference results by pathology, 57 lesions were categorized as O-RADS 3 by US, 18 of them were diagnosed as malignant according to pathology. Out of 51 lesions categorized as O-RADS 4 by US, 30 were diagnosed as benign by pathology as shown in Table 3.

Fig. 2

A 37-year-old female patient presented with pelvic pain, fever, and leukocytosis. a transvaginal ultrasound showing left adnexal well defined bilocular cystic lesion of turbid content measures about 5 × 3 cm. b color Doppler study shows peripheral vascular activity. Scoring: O-RADS US 3 color Score 2. Diagnosis by pathology: tubo-ovarian abscess

Fig. 3

A 16-year-old female patient presented with pelvic pain and abdominal distension. a Large left pelvi-abdominal mixed soft tissue/cystic mass lesion measures about 8 × 10 cm the cystic component is multiloculated with turbid content & thick internal septations b power doppler study showing internal flow is detected. Scoring: O-RADS US 4— color score 2. Diagnosis by pathology: left ovarian juvenile granulosa cell tumor

Fig. 4

A 52-year-old female patient presented by postmenopausal bleeding transvaginal ultrasound reveals large pelvic right soft tissue mass lesion measures about 10 × 7 cm with moderate vascular activity on color doppler. Score: O-RADS US 4, color score = 3. Diagnosis by pathology: pedunculated subserous leiomyosarcoma

Fig. 5

A 49-year-old female patient presented by irregular bleeding and pelvic pain a TAS shows unilocular left adnexal complex cystic lesion with solid component noted anterosuperior score: O-RADS US 4 CS:2. Diagnosis by pathology: endometrioid adenocarcinoma

Table 3 O-RADS classification by US in relation to pathology results

In 44.4% of the investigated masses, no blood flow was detected using the color doppler score, which was based on the strength of the color signal, minimal flow in 36.1%, moderate flow in 11.1%, and high vascular flow in 8.3% as shown Fig. 6.

Fig. 6

O-RADS color score of the studied patients

At cutoff 4, the O-RADS US score for malignancy gave a sensitivity of 93.13% (95% CI 25.13–80.78), specificity of 66.72% (95% CI 34.49–76.81), PPV of 93.18% (95% CI 26.07–58.16), and NPV of 75.42% (95% CI 52.13–81.17) with an overall accuracy of 92.56% (95% CI 38.10–72.06) as summarized in Table 4.

Table 4 Diagnostic performance of O-RADS US score for malignancy according to pathology results

Discussion

When an adnexal lesion is noticed on pelvic ultrasound examination, the objective is to classify this lesion as benign versus potentially malignant when it is found during a pelvic ultrasound examination to help with the necessary follow-up, which may include a possible referral to gynecology oncology. To further assist radiologists in classifying and recommending treatment for women with adnexal lesions, the ACR O-RADS Committee has released the O-RADS US Risk Stratification and Management System [10].

The current study included 108 females with sonographically indeterminate adnexal masses, with ages ranging between 16 and 62 years (mean age of 42.92 ± 13.01 years). Most patients (91.7%) were married. Out of 108 patients, 61.1% were premenopausal& 38.9% were postmenopausal.

Similarly, Hack et al. [11] performed research including all women who had pelvic US at a tertiary referral cancer hospital between August 2015 and April 2017. As many as 2801 pelvic US studies were found during the study period, and 227 individuals with 262 lesions (9 percent) were included. There was a wide range of ages represented, with 52 being the mean. In terms of when they entered and exited menopause, the breakdown was as follows: 113 (50% of the sample) were postmenopausal, 107 (47%) were premenopausal, and 7 (2% of the sample) were perimenopausal (3 percent) [11].

Also, AMOR. [12] found that adnexal masses were more common in postmenopausal elderly women [12].

In the current study, we found that all 108 patients suffered from pain, more than half of patients (63.9%) suffered from constipation or diarrhea, 44.4% had a fever, 41.7% had palpable mass or increased abdominal volume, 22.2% had vaginal bleeding, and 19.4% had urinary symptoms. This agreed with Bhagde et al. [13], who stated that about 92% of patients complained of stomach aches [13].

Furthermore, Givens et al. [14] showed that women with ovarian cancer most often have pelvic or abdominal discomfort [14].

On the other hand, ovarian cancer often has vague symptoms such as IBS, lethargy, and sudden weight loss [15, 16].

In the current study, we cleared that based on the O-RADS US score, more than half masses (52.8%) were diagnosed as O-RADS 3, which is low-risk malignant, and 47.2% were diagnosed as O-RADS 4 being intermediate-risk malignant.

Concurrently, Zhang et al. [17] examined 263 masses using U/S GIRADS and discovered that 86 of them were benign neoplasm (GI-RADS 3), while 101 were of GI-RADS 4 [17].

The GIRADS classification was used to determine the severity of 112 lesions, and the results showed that 32 lesions (28.6%) were GI-RADS 3, and 13 lesions (11.6%) were GIRADS 4 [14].

In the current study, we demonstrated that regarding US O-RADS classification in relation to the reference results by pathology, 57 lesions were categorized as O-RADS 3 by the US, and 3 of them was diagnosed as malignant according to pathology (false negative). Out of 51 lesions categorized as O-RADS 4 by the US, 42 were diagnosed as benign by pathology (false positive).

Our study results are in agreement with the results of the study done by Zhang et al. [17] results which found 4 false-negative malignant cases that were misclassified as GI-RADS3, whereas 24 benign lesions with false-positive results that were diagnosed as GI-RADS 4 [17].

In the current study, we demonstrated that based on pathology results which were the reference standard, 36.1% of the total adnexal masses were malignant.

Zhang et al. [17] results. They looked at 242 individuals with tumors of varying malignancy (110 cancerous and 153 benign) [17].

Unlike the findings of Pereira et al. [18], that identified a significant malignancy rate, with 90 (47.37%) of 190 masses meeting the criteria for malignancy based on histological examination [18].

Adnexal lesions with a typical appearance may be reliably detected and characterized by transvaginal sonography. But in the 2 biggest ovarian cancer screening studies, a considerable percentage of false-positive individuals received unnecessary surgery [19, 20]. The accuracy and specificity of an ultrasound examination may be diminished if the patient has nonclassical traits including avascular solid components, a big mass, or if the sonographer is inexperienced. The risk of malignancy index, the risk of ovarian malignancy algorithm, and other sonographic grading methods have all been endorsed. However, results have been mixed in actual clinical settings, maybe because of variations in operator experience and cancer prevalence within the study group [19, 20].

In this study, we found that at cutoff 4, the O-RADS US score for malignancy gave a sensitivity of 93.13% (95% CI 25.13–80.78), specificity of 66.72% (95% CI 34.49–76.81), PPV of 93.18% (95% CI 26.07–58.16), and NPV of 75.42% (95% CI 52.13–81.17) with an overall accuracy of 92.56% (95% CI 38.10–72.06).

There is a concordance between our findings and those of Prasad et al. [21], which came to the conclusion that histology and U/S O-RADS had excellent agreement for the diagnosis of benign and malignant ovarian tumors, with 100% sensitivity, 80% specificity, 36% PPV, and 100% NPV, at cutoff point 0.6 [21]. Our study had some limitations. The sample size was relatively small. This explains that our study did not include less common but not rare adnexal lesions, i.e., ovarian edema, ovarian torsion, and inflammatory ileocecal masses as a mimic of adnexal lesion. In addition, 57% of our patients had histopathological examination of their lesions, which is considered the definite diagnostic test. As the remaining patients (36%) were treated conservatively with regular follow-up with either regressive or stable lesions supporting the radiological diagnosis with MRI and TVUS examination.

Conclusions

The US O-RADS classification system is a crucial non-invasive diagnostic tool for suspicious ovarian masses with high sensitivity in differentiation between benign and malignant neoplastic lesions.