Diagnostic value and agreement of transrectal in comparison with transvaginal sonography among women with abnormal uterine bleeding

Aims Transvaginal sonography (TVS) is not applicable for evaluating the endometrium in some cases with abnormal uterine bleeding (AUB) such as virgin women. The aim of the present study was to investigate the diagnostic value of transrectal sonography (TRS), as a non-invasive alternative for TVS, among women with AUB.

In this cross-sectional study, 40 women over 40 years of age with AUB first underwent TRS and then TVS. Endometrial biopsy was also performed as a gold standard method to evaluate endometrial pathologies. The findings of the two endometrial ultrasound methods were compared with the biopsy results. Also, the findings of the two methods were compared in terms of the agreement on other uterine markers and adnexal findings.

There was a high agreement between the findings of TVS and TRS for uterine size, endometrial thickness and homogeneity, endomyometrial junction, myometrial homogeneity, uterine lesions, uterine lesions size, ovarian size and ovarian echogenicity. When comparing the results of these two methods with biopsy findings, sensitivity, specificity as well as positive and negative predictive values of both methods were similar (82%, 100%, 100%, and 0%, respectively).

When it is not possible to use TVS in women with AUB, TRS is a suitable, non-invasive and inexpensive alternative method for evaluating the endometrium and other genital organs.

Abnormal uterine bleeding, Transvaginal sonography, Transrectal ultrasonography, Endometrium, Pipelle

According to the American College of Obstetricians and Gynecologists (ACOG) some causes of abnormal uterine bleeding (AUB) include problems with ovulation, fibroids, polyps which cause the endometrium to grow into the wall of the uterus, bleeding disorders, problems linked to some birth control methods such as intrauterine devices (IUD) or birth control pills, miscarriage, ectopic pregnancy and certain types of cancer, such as cancer of the uterus. Any significant deviation from a woman’s established menstrual pattern may be considered abnormal uterine bleeding, and several factors direct the evaluation of a patient with such bleeding. Premenopausal disorders that can be well evaluated using ultrasound (US) include endometriosis, adenomyosis, and leiomyomas. A positive pregnancy test in a woman of childbearing age prompts a search for an intrauterine pregnancy. Possible complications that may contribute to bleeding include ectopic pregnancy; placental factors including position, trauma, and infection; gestational trophoblastic diseases; preterm labor; and postpartum complications. Atrophic changes, hormonal status, and carcinoma are some other considerations in a postmenopausal patient with abnormal uterine bleeding. Foreign bodies, trauma, infection, polyps, and iatrogenic causes can be observed in all groups. Differential diagnoses for abnormal uterine bleeding in premenopausal, pregnant, and postmenopausal patients are well evaluated with US, and US techniques have greatly facilitated the evaluation of pelvic diseases. Urgent and emergent conditions such as ectopic pregnancy, placenta previa, and preterm labor are readily identifiable using US [1]. Abdominal examination for tenderness, masses, distension, pelvic/perineal examination using vaginal exam, speculum exam, pap smear, cervical cultures if there is a concern for STI and rectal exam if there is a concern for rectal source of bleeding is recommended. In girls with intact hymen, rectal examination is a common method for assessing pelvic organs. The most common gynecologic malignancy among American women is endometrial cancer [2]. In Iran, according to previous studies, uterus cancer has been recognized as the fifth prevalent cancer among females [3]. Fortunately, early detection of the disease is associated with an increase in survival rate of up to 95% [4]. Since 1843, diagnostic dilation and curettage (D&C) has been a standard method for diagnosis of endometrial cancer. In 1970's endometrial biopsy with Pipelle was introduced as a cheap and simple method for endometrial sampling without anesthesia [5]. Another method for evaluating uterus malignancies is the use of trance vaginal sonography (TVS). Although in many women uterine cavity and pelvic evaluation is possible using (TVS), it cannot be performed in some cases, such as women with vaginismus, congenital or secondary vaginal stenosis, virgins, and in cultures which vaginal examination is not acceptable before marriage. On the other hand over recent decades, with the rising age of marriage among Iranian women, as in many other countries in the world, the number of maidens more than 40 years old with AUB has increased. In these patients the possibility of trauma to an intact hymen limits the use of TVS, endometrial biopsy with Pipelle or curettage, or hysteroscopy for necessary diagnostic evaluations. Consequently, trans-abdominal ultrasound (TAS) is often used to evaluate the genital organs among these patients, with lower sensitivity and specificity compared to TVS for detecting the uterine lesions [6]. In such cases, the use of transrectal ultrasound (TRS) has been proposed as a non-invasive and inexpensive alternative to TVS for the evaluation of uterine pathologies [7]. The purpose of our study was to answer the question of whether it is possible to use TRS as a useful, accessible, inexpensive, non-invasive and reliable tool for gynecological disorders diagnosis in women who cannot be checked by TVS or not. The main advantage of this study is finding an alternative way for diagnosing the cause of bleeding in virgin girls and all other women who for any reason can not be examined vaginally. In the present study, which is to the best of our knowledge the first trial of its kind in Iran, the diagnostic value of TRS was compared with TVS for diagnosis of endometrial pathologies, among married (non virgin) women over 40 years of age with AUB. Also, a comparison was made with regard to the agreement between TRS and TVS in assessing the myometrial and adnexal pathologies.

This cross-sectional study, included women referred to the clinics of three university hospitals in Tehran, Iran, (Shahid Akbar-Abadi hospital, Firoozgar hospital and Imam Hossein Medical Center), with abnormal uterine bleeding between August 2020 and February 2021. The inclusion criteria were as follow: non virgin women over 40 years of age who had abnormal uterine bleeding within 3 months before referral. The exclusion criteria included virginity, vaginismus, history of endometrial cancer, diagnosis and treatment for carcinoma in situ, previous hysterectomy, abnormal results in Pap smear (ASC-US, AGC, LSIL, ASC-H, HSIL, AIS, or cervical cancer) and those with acute pelvic inflammatory diseases. Also, women who did not accept transvaginal or transrectal sonography were excluded from the study. The sample size of 40 patients was estimated using the data from a previous study by Alcazar et al., and based on the sensitivity of transvaginal/transrectal ultrasound for producing a two-sided 95% confidence interval [8]. To evaluate the agreement between the two ultrasound methods a sample size of 40 subjects can achieve 80% of the power of the test using the Kappa statistics. All patients received informed written consent before inclusion in the study, and patients who did not wish to continue were allowed to leave the study at any stage. The study was approved by the Ethics Committee of Iran University of Medical Sciences (IR.IUMS.REC.1399.370). After obtaining the history and recording the demographic data of patients including age, pattern and duration of abnormal bleeding, associated underlying diseases and Pap smear findings, all patients underwent genital examination with speculum and bimanual vaginal and rectovaginal examinations. Then, all patients were referred to the radiology department of Imam Hossein Medical Center for sonography. All patients were subjected to TRS by a radiologist with experience in the field of TRS and then TVS was performed by another radiologist expert in gynecologic imaging and blinded about the TRS results. All findings from each sonography were recorded in separate forms. The ultrasound apparatus used in this study was an Esaote (Mylab™ 50) device and an endocavitary two-part probe. After ultrasonography, endometrial biopsies using Pipelle were performed for all patients by a gynecologist. Endometrial biopsy samples were sent to the pathology department of Shahid Akbar-Abadi Hospital for histopathological evaluation and the results of all samples were recorded. Statistical analysis Data was analyzed using R software (Version 3.4.1). Student T test was used to determine the difference between normal quantitative variables and MacNemar’s test was used for qualitative variables. The agreement level of TRS and TVS was estimated using Cohen’s Kappa and prevalence-adjusted and bias-adjusted Kappa (PABAK) statistics. The quantitative variables were reported using mean ± standard deviation and the significance level was set at 0.05. Cohen’s kappa, symbolized by the lower case Greek letter, κ [9] is a robust statistic method useful for either interrater or intrarater reliability testing. Similar to correlation coefficients, it can range from − 1 to + 1, where 0 represents the amount of agreement that can be expected from random chance, and 1 represents perfect agreement between the raters. While Kappa values below 0 are possible, Cohen notes they are unlikely in practice [9]. As with all correlation statistics, the Kappa is a standardized value and thus is interpreted the same across multiple studies.Cohen suggested the Kappa result should be interpreted as follows: values ≤ 0 as indicating no agreement, values between 0.01 and 0.20 as none to slight agreement, values between 0.21 and 0.40 as fair agreement, values between 0.41 and 0.60 as moderate agreement, values between 0.61 and 0.80 as substantial agreement, and values between 0.81 and 1.00 as almost perfect agreement [10].

A total of 40 eligible women were enrolled in the study. The mean age of women was 47.9 ± 1.1 years. Of the participants, 32 patients (80%) were pre-menopausal and 8 (20%) were menopausal. The abnormal uterine bleeding pattern of the studied patients is presented in Fig. 1. Regarding the underlying conditions, six patients (15%) had hypertension, two patients (5%) had diabetes, one patient (2.5%) had hypothyroidism, and the rest had no underlying diseases. The mean thickness of the endometrium was 8.01 ± 5.3 mm in the transvaginal method and 7.95 ± 5.2 mm in the transrectal method. There was no statistically significant difference between the findings of the two methods (P = 0.395). In the histopathologic evaluation of endometrial samples, the following results were obtained: 4 cases of chronic endometritis, 7 cases of endometrial polyp, 4 cases of secretary endometrium, 1 case of asynchronous endometrium, 4 cases of cystic hyperplasia, 11 cases of proliferative endometrium and 9 cases of atrophic endometrium. Table 1 shows the Patient’s characteristics, imaging and pathological findings. In Table 2, the strengths of agreement for other gynecological ultrasound findings from transrectal and transvaginal methods have been shown. The agreement proportions of the two methods considering the uterine size, homogenicity of myometrium, endomyometrial junction, uterine structural abnormities including leiomyoma, polyps and congenital anatomical anomalies, right and left ovarian size and echogenicity, right and left ovarian lesions and fluid or pathological lesions in cul-de-sac were very high (Table 2). This agreement for the endometrial homogenicity was high (Table 2). Table 3 shows the association between transvaginal and transrectal ultrasonography in comparison with the histopathologic results of endometrial biopsy, as the gold standard method. Sensitivity, specificity, positive and negative predictive values of these two methods in diagnosis of endometrial lesions is shown in Table 3. As shown in this table, the sensitivity, specificity, positive and negative predictive value of both methods in evaluating endometrial lesions, compared to the biopsy as the gold standard, were 82.5%, 100%, 100%, and 0%, respectively, (Figs. 2, 3). Table 1. | Variable | N | Percent | Mean | |---|---|---|---| | Age | 40 | 100 | 1.1 ± 47.9 | | Contraception method | ||| | Withdrawal | 11 | 27.5 | – | | Condom | 10 | 25 | – | | Tubal ligation | 7 | 17.5 | – | | Calendar rhythm | 7 | 17.5 | – | | DMPA | 2 | 5 | – | | OCP | 1 | 2.5 | – | | IUD | 1 | 2.5 | – | | Vasectomy | 1 | 2.5 | – | | Menopause status | ||| | Postmenopausal | 8 | 20 | – | | Premenopausal | 32 | 80 | – | | Underlying disease | ||| | No underlying disease | 31 | 77.5 | – | | Hypertension | 6 | 15 | – | | Diabetes | 2 | 5 | – | | Hypothyroidism | 1 | 2.5 | – | | Ultrasound findings: uterine position | ||| | Retroverted | 4 | 10 | – | | Antroverted | 18 | 45 | – | | Normal | 18 | 45 | – | | Ultrasound findings: adnex status | ||| | Normal | 29 | 72.5 | – | | With cyct | 8 | 20 | – | | Endometrioma + hematosalpinx | 1 | 2.5 | – | | Atrophic | 2 | 5 | – | | Pathological findings | ||| | Chronic endometritis | 4 | 10 | – | | Polyp | 7 | 17.5 | – | | Secratory endometrium | 4 | 10 | – | | Prolifrative endometrium | 10 | 25 | – | | Asynchronously developed endometrium | 1 | 2.5 | – | | Inactive endometrium (atrophic) | 9 | 22.5 | – | | Cystic hyperplasia | 3 | 7.5 | – | | Submucosal myoma + prolifrative endometrium | 1 | 2.5 | – | | Adenomysis and lyomyoma | 1 | 2.5 | – | DMPA depot-medroxyprogesterone acetate, OCP oral contraceptive pill, IUD intrauterine devices, HTN hypertension Table 2. | Ultrasound Finding | Concordance | Discordance | Cohen’s Kappa | PABAK | P value* | |---|---|---|---|---|---| | Uterine Size | 100% (40) | 0% (0) | 1 | 1 | < 0.001 | | Endometrial Homogeneity | 92.5% (37) | 7.5% (3) | 0.756 | 0.85 | < 0.001 | | Endometrial Morphology | 95% (38) | 5% (2) | 0.883 | 0.9 | < 0.001 | | Myometrial Homogeneity | 95% (38) | 5% (2) | 0.898 | 0.9 | < 0.001 | | Endo-myometrial Junction | 95% (38) | 5% (2) | 0.848 | 0.95 | < 0.001 | | Uterine Lesions | 95% (38) | 5% (2) | 0.916 | 0.9 | < 0.001 | | Size of Right Ovary | 100% (40) | 0% (0) | 1 | 1 | < 0.001 | | Size of Left Ovary | 100% (40) | 0% (0) | 1 | 1 | < 0.001 | | Echo of Right Ovary | 100% (40) | 0% (0) | – | 1 | – | | Echo of Left Ovary | 100% (40) | 0% (0) | – | 1 | – | | Lesions of Right Ovary | 100% (40) | 0% (0) | 1 | 1 | < 0.001 | | Lesions of Left Ovary | 100% (40) | 0% (0) | 1 | 1 | < 0.001 | | Cul-de-sac Fluid | 100% (40) | 0% (0) | – | 1 | – | The PABAK meaning is Prevalence-Adjusted Bias-Adjusted Kappa *The P values were calculated based on McNamara’s test Table 3. | Test | Pathology result (n = 40) | PABAK | Sensitivity (95% CI) | Specificity (95% CI) | PPV (95% CI) | NPV (95% CI) | ||| |---|---|---|---|---|---|---|---|---|---| | TP | FP | FN | TN | |||||| | Transvaginal | 82.5% (33) | 0% (0) | 17.5% (7) | 0% (0) | 0.65 (0.34, 0.85) | 82.5% (67.2, 93.6) | 100% (NA) | 100% (89, 100) | 0% (0, 41) | | Transrectal | 82.5% (33) | 0% (0) | 17.5% (7) | 0% (0) | 0.65 (0.34, 0.85) | 82.5% (67.2, 93.6) | 100% (NA) | 100% (89, 100) | 0% (0, 41) | PABAK prevalence-adjusted and bias-adjusted kappa, PPV positive predictive value, NPV negative predictive value, NA not available, TP true positive, FP false positive, FN false negative TN true negative

In the present study we examined the diagnostic value of transrectal sonography and transvaginal sonography in comparison to histopathologic findings as the gold standard, in married (Non virgin) women over 40 years of age with abnormal uterine bleeding (AUB). Age of over 40 years is a known risk factor for endometrial diseases [11]. It should be noted that there is general inconsistency in the nomenclature used to describe abnormal uterine bleeding (AUB), in addition to a plethora of potential causes; several of which may coexist in a given individual [12]. In our study there was a High agreement between the findings of transvaginal and transrectal ultrasound in terms of uterine size (1 = Choen Kappa), endometrial thickness and homogeneity (Choen Kappa = 0.756), junction between endometrium and myometrium (Choen Kappa = 0.883), myometrial homogeneity (Choen Kappa = 0.898), The presence of uterine lesions (Choen Kappa = 0.916), the size of uterine lesions (Choen Kappa = 1) and the size (Choen Kappa = 1) and ovarian echo (Choen Kappa = 1). Although previous studies have reported similar results the however this findings are important given the setting of our study in Iran. The sensitivity, specificity, positive and negative predictive value of both methods in evaluating endometrial lesions, compared to the biopsy as the gold standard, were 82.5%, 100%, 100%, and 0%, respectively. TVS as a diagnostic method is not possible to use in many cases of AUB. Some examples of this condition are the presence of vaginismus, vaginal stenosis due to congenital or iatrogenic problems and evaluation of genital organs among virgin adolescents and unwilling maidens, especially in cultures which vaginal examination is not acceptable before marriage. Also there are problems associated with vaginal sonography during active and severe uterine bleeding (Figs. 4, 5). On the other hand, hypoestrogenism causes the fragility of the mucosa which increases the risk of tears and discomfort during TVS, which makes TRS a potential candidate as an alternative method in postmenopausal women. In most of these cases, transabdominal ultrasound (TAS) is often performed instead of the TVS method. In a previous study TVS had a higher value compared to TAS in detecting uterine lesions [13]. According to our results, there was very high agreement between TRS and TVS in evaluating uterine size and its lesions. Also, according to the findings of our study, there was no clear superiority in terms of diagnostic value between TRS and TVS. Therefore, in assessing uterine lesions, TRS has a higher diagnostic value than TAS and is a better alternative in cases where vaginal sonography is not possible. In our study, there was no statistically significant difference between TVS and TRS ultrasound findings in terms of endometrial thickness, so it seems that TRS might be as good as TVS for the evaluation of endometrial thickness. According to the results of Bazot et al., study, as in our study, two methods of ultrasound did not show a significant difference in the evaluation of endometrial thickness and also the diagnosis of pelvic endometriosis [14]. In our study, the diagnostic value of transvaginal and transrectal ultrasonography in endometrial evaluation was compared to the results of endometrial biopsy, with the exception that we used the simpler and less aggressive Pipelle method instead of D&C for endometrial biopsy. In our study, the sensitivity (82%) and specificity (100%) of TVS and TRS methods for detection of endometrial lesions were the same. Sawicki et al., compared TVS to D&C and reported that its accuracy was more than 91%, while the sensitivity and specificity of ultrasonography in measuring the endometrial homogenicity was 90% and 97%, respectively [15]. In our study, the agreement between transrectal and transvaginal methods was high for endometrial homogeneity and very high for endometrial morphology. In the present study, there was an agreement of 91% for the examination of uterine lesions and 100% for the assessment of ovarian size between transrectal and transvaginal ultrasonography. A study by Wachsberg et al., also concluded that there is a high agreement between the two methods in determining uterine lesions, and if the uterus is placed in retroverted state, the sensitivity of TRS is even greater than the TVS sonography [11]. In our study, we did not use standard surgical methods for assessing adnexal lesions; therefore a comparison of TRS with TVS was performed. Lee et al. concluded that TRS was as effective as TVS in evaluating the polycystic ovaries [16]. The high agreement rates between TRS and TVS regarding the ovarian parameters in our study confirms the findings of the study by the Lee et al., TRS scanning should be used liberally after proper patient selection and counseling [17]. TVS might be superior to TAS, especially in patients with a retroflexed uterus [18]. In general, based on the findings of this study, transrectal ultrasound has a high sensitivity and specificity in the diagnosis of endometrial lesions. Also, to evaluate the adnexa, the sonographic findings in the transrectal method have a very high agreement with the transvaginal method. Therefore, in cases such as the presence of virginity which makes the use of TVS to assess the uterus, endometrium and adnexa impossible, TRS is recommended as an easy, outpatient and non-invasive method with similar diagnostic value (Figs. 6, 7, 8).

This study has several limitations. One limitation was that the two techniques used in this study were performed by different operators. Also in our study, the consensus between TRS and TVS methods was high for endometrial hemogenesis and very high for endometrial morphology. Therefore, it seems that TRS can be a valuable diagnostic tool when there is a high clinical suspicion of endometrial cancer and no TVS is available or possible. However, based on histopathologic findings no cases of endometrial cancer were found among our patients. Therefore, based on the findings of the present study, we cannot reliably comment on diagnostic value of TRS in identifying endometrial cancer. It is suggested that future RCT studies with a higher sample size evaluate the accuracy of TRS compared with TVS in patients with endometrial cancer confirmed with biopsy (Figs. 9, 10, 11).

Generally, according to our findings, TRS shows a high sensitivity and specificity in diagnosis of endometrial lesions. Also, ultrasound findings in the TRS method show very high agreement with TVS method when evaluating myometrial and adnexal problems. Therefore, TRS is recommended as an easy, outpatient and noninvasive diagnostic tool in conditions like virginity, which does not allow the use of transvaginal sonography to evaluate the uterus, endometrium and adnexa (Fig. 12). In conclusion based on the results of the present study, when it is not possible to use TVS in women with AUB, the use of TRS is a suitable, non-invasive and inexpensive alternative method for evaluation of endometrium and other genital organs.

The authors would like to thank the Shahid Akbarabadi Clinical Research Development Unit (ShACRDU), Iran University of medical sciences (IUMS), Tehran, Iran, for their non-financial supports throughout the period of study. Abbreviations - TVS Transvaginal sonography - AUB Abnormal uterine bleeding - TRS Transrectal sonography - D&C Diagnostic dilation and curettage - TAS Trans-abdominal ultrasound - PABAK Prevalence-adjusted and bias-adjusted kappa - AURC Area under the ROC curve Author contributions All authors have contributed significantly to the manuscript: AAS: data analysis, preparing manuscript. FF: study design and supervision. AM: gathering data, endometrial sampling. AMF: performing trans-vaginal and trans-rectal ultrasounds. AA: statistical analysis. SRSM: review. EG: review. All authors have read and approved the manuscript. Funding None. Availability of data and material Available if required. Declarations Conflict of interest The authors have no conflict of interest with the subject matter of the present study. Ethics approval and consent to participate All patients received informed written consent before inclusion in the study, and patients who did not wish to continue were allowed to leave the study at any stage. The study was approved by the Ethics Committee of Iran University of Medical Sciences (IR.IUMS.REC.1399.370). Consent for publication The study has been submitted to Journal of Ultrasound for publication after review process. The manuscript has not been published or submitted for publication elsewhere. Footnotes Publisher's Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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