ROLE OF ROUTINE COMPREHENSIVE SYSTEMATICPELVIC LYMPHADENECTOMY IN THE MANAGEMENT OF ENDOMETRIAL CANCER: A RETROSPECTIVE COHORT STUDY

ROLE OF ROUTINE COMPREHENSIVE SYSTEMATICPELVIC LYMPHADENECTOMY IN THE MANAGEMENT OF ENDOMETRIAL CANCER: A RETROSPECTIVE COHORT STUDY

By

Butheina Khalil Gerriw¹, Awatif Mohamed Abousahmeen², Mohammed Ahmed BenSaud^3, Ebtihaj Taher Hassan⁴, Suad Issa Zayid⁵, Mohanad Taher Bentaher^6, Nahla Ibrahim Betelmal⁷

1-Department of Gynecology, Libyan International Medical University, Benghazi, Libya. 2, 3- Department of Radiotherapy, National Cancer Institute, Misurata, Libya.  4-Department of Radiotherapy, Tripoli University Hospital. 5- Department of Radiotherapy, National Cancer Institute, Sabratha, Libya. 6-Misurata University, Libya.  7-Statistical Researcher, Glasgow Caledonian University, Glasgow UK.

Correspondence:bouthinagreiw@gmail.com. Gynecology Department Libyan International Medical University, Benghazi, Libya

ABSTRACT

Background: Endometrial cancer is the fifth most common cancer among women worldwide. Systematic lymphadenectomy of pelvic lymph nodes (LN) and para-aortic are often part of surgical staging. This procedure is not done universally. The therapeutic effects of lymphadenectomy are issues of great debate.Complications of lymphadenectomy including lymphadenoma and lymphatic cysts can affect patients’ quality of life.

Objective: To evaluate the use of systematic pelvic lymphadenectomy in the management of endometrial cancer.

Patients and Methods:  A descriptive retrospective cohort study was conducted in multi-centric three national cancer institutes (Tripoli, Misurata, and Sabratha) located at Western -Northern Libya, from January 2020 toMay2022. A total number of 180 diagnosedendometrial cancer cases were enrolled in the study.In all cases routine systematic pelvic lymphadenectomy was conducted. Theprimary outcome measure was the rate of lymph node metastases in relation to tumor (size, depth of endometrial invasion, grade, histopathological findings, and lymph-vascular space invasion) and patients’ characteristics (age, parity, co-morbidities including obesity).

Results: There was no significant association between lymph nodemetastasis and patients’ characteristics.Patients were divided into two groups: below sixty years old and above sixty,menstrual status into perimenopausal, and postmenstrual,parity, nullipara, and multipara, obesity body mass index (BMI) below 25 and above 25, and presence or absence of comorbidities.

There were significant associations with all tumor factors except tumor size.Stage Irepresented nearly 60% of sample (59.44%), stage II 18.9%, stage III 18.3%, and stage IV (3.3%). Low risk patients (FIGO stage I, grade 1-2) had 6.52% lymph node, intermediaterisk (FIGO stage II, any grade) had 17.65% lymph node invasion, and high risk (FIGOIII, and FIGO IV 84.8%, and 100% respectively. (The overall incidence of lymph node metastasis in clinically uterine-confined endometrial cancer was proportionally increasing with the increase in gradings. (About9% in grade 1, 19% in grade 2, and 76% in grade 3).Lymph node metastasis occurred in 11% of cases with less than 50% myometrial invasion,compared with about 38% of patients with more than 50% myometrial invasion.Histopathologicallymore invasion occurred with poorly differentiatedtumors(64%), and the least occurred with endometrioid carcinoma (23%). Lymph-vascular space invasion significantly affected lymph node metastasis, it occurred in 15.2% of low risk group (FIGO stage I) was highest (100%) in high risk group (FIGO stage IV).

Conclusion:Use of more precise and less aggressive methods may be useful to predict tumor aggressiveness and lymph node metastasis. Such methods include preoperatively theuse ofmolecular markers, computerized tomogram scan(CT), magnetic resonance images (MRI), ultrasound scanning, and the intra-operatively use of sentinel lymph nodes mapping during surgical procedures. These investigations should be considered to assess ovarian, nodal, peritoneal, and other sites of metastatic disease.

Key words: Endometrium cancer, pelvic lymphadenectomy, prognostic factors.

INTRODUCTION

Endometrial cancer is the fifth most common cancer among women worldwide (Frostet al.,2017). Endometrial cancer has been classified into two main clinicopathologicaltypes:type I is the more common endometrioid adenocarcinoma (80%–90%), and type II comprises non-endometrioid subtypes such as serous, clear cell and undifferentiated carcinomas, as well as carcinosarcoma/malignant-mixed Müllerian tumor (10%–20%)(Colombo et al.,2016).Most cases of endometrial cancer present with early-stage disease (90%), without metastasis(Khouryet al., 2016).

Risk factors are related to excessive unopposed exposure of the endometrium to estrogen, including unopposed estrogen therapy, early menarche, late menopause, tamoxifen therapy, nulliparity, infertility or failure to ovulate, and polycystic ovary syndrome. Additional risk factors are increasing age, obesity, hypertension, diabetes mellitus, and hereditary nonpolyposis colorectal cancer(Braun et al., 2016).

Astudy in westernLibyastated that the most common malignanciesin women were breast and uterine cancer. In Libya the standard of treatment of endometrial cancerconsists of hysterectomy and bilateral salpingo-oophorectomy, and includescomprehensive systematic pelvic lymphadenectomy which is done routinely during the surgical procedure for staging, and as treatment option(Ismail et al., 2021).

Systematic lymphadenectomy of pelvic lymph nodes is used with paraaortic lymphadenectomy selectively or routinely in USA and Japan. This procedure is not done universally, in the United Kingdom, where lymphadenectomy is not a common procedure. The therapeutic effects of lymphadenectomy are an issue of great debate (Todo et al., 2010).Comprehensive lymphadenectomy result in prolonged operating time which leads to many complications, including wound infection, hemorrhage, vascular and nerve injury, and complications of prolonged anesthesia. (Khoury et al., 2016).

Other acceptable surgical strategies between a complete lymphadenectomy and no nodal evaluation in patients with endometrial cancer, including Sentinel Lymph Nodal (SLN) mapping (imaging procedure lymphography). This approach is based on the concept that lymph node metastasis is the result of an orderly process; that is, lymph drains in a specific pattern away from the tumor, and therefore, if the SLN, or first node, is negative for metastasis, then the nodes after the SLN should also be negative(Smith, 2017).Sentinel lymph node mapping is feasible and accurately predicts nodal status in women with endometrial cancer. The current data favors the use of cervical injection techniques with indocyanine green. Sentinel lymph mapping may be considered an alternative standard of care in the staging of women with endometrial cancer(Accorsi et al., 2020).

The aim of the current study was to examine the need for routine pelvic systematic lymph node dissection in the management of endometrial cancer,and to focus on the relation between lymph node metastasisand both prognostic factors (myometrial invasion, tumor grade, FIGO stage, lymph vascular space invasion) andpatients’ characteristics.

PATIENTS AND METHODS

A descriptive retrospective cohort study was conducted in multi-centric three national cancer institutes (Tripoli, Misurata, and Sabratha) located at Western -Northern Libya, from January 2020 to May2022. A total number of 180 cases were enrolled in the study. The primary outcome measure was the rate of lymph node metastases in relation to tumor and patients’ characteristics

Women were diagnosed as having endometrial cancer and received surgical treatment including hysterectomy and bilateral salpingo-oophorectomy.  Routine systematic lymphadenectomy was done routinely in all the patients in the three cancer institutes with systematic pelvic lymphadenectomy included resection of the internal iliac nodes, external iliac nodes, medial deep inguinal nodes, obturator nodes, common iliac nodes,and circumflex iliac node resection.

Pelvic lymph nodes metastasis was studied in relation to patients’and tumorcharacteristics and divided into two groups: below sixty years old and above sixty,menstrual status into perimenopausal, and postmenstrual,parity, nullipara, and multipara,obesity body mass index (BMI) below 25 and above 25, and presence or absence ofcomorbidities.

Tumor factors include, size, depth of myometrial invasion,histopathology, FIGO classification, grading and,lymph vascular space invasion.

Statistical Analysis:

Association of variables with lymph nodes (LN) Metastases was assessed with Chi-Square test, χ² test. Data were represented as frequencies and percentages. Odds ratio were estimated by the Logistic regression. The odds ratio compares the odds of two events: presence/occurrence of LN Metastases and absence of LN Metastases.P values of less than 0.05 were considered significant.

RESULTS

One hundred and eighty (180) patients with malignant tumors of the uterine corpus had been registered in three cancer treatment institutions in Libya: Tripoli (n=77, 43%), Misurata (n=38, 21%) and Sabratha (n=65, 36%). Regarding patients’ characteristics in relation to lymph node metastasis in the study sample, patients less than   60 years represented 55% (99 cases, lymph node metastasis was present in quarter of them (28%), while lymph node metastasis was present in one third of cases (31%) over sixty years old.

Peri-menopausal patients nearly quarter of the sample, 27% of them with nodal metastasis. While 30% of postmenopausal had nodal metastasis. Parity: nulliparity was in nearly half the sample with nodal metastasis in quarter of them (27%). While nodal metastasis found in third of multipara patients.54% of the sample have one or more comorbidities such Hypertension and Diabetes Miletus, however, only 20% of the sample has a family history of malignancies. 74% of the sample is obese with BMI>25. In terms of Histopathological types of Endometrial cancer: Endometrioid (n=142, 79%), Poorly Differentiated (n=14, 8%), Serous (n=12, 7%), Sarcoma (n=11, 6%) and one case of Mucinous (Figure 1).

The probability of a patient with LN metastasis was the same across patient characteristics and tumor factors (Table 1). There was no significant association between LN metastasis and patients’ characteristics. However, there was a significant association with all tumor factors except tumor size.

Table (1): Patient Parameters and Tumor factors in relation to Pelvic Lymph Node Metastasis

Out of the 180 patients there were 53 cases (29%) that show positive LN Metastasis. Patients had been categorized into different groups based on International Federation of Gynecology and Obstetrics (FIGO) stages and Tumor Grade (Table 2). Table 3 shows Lymph Node Metastasis and Lymph-vascular space invasion (LVSI) distribution according to Risk classification respectively.

Table (2): FIGO Staging of Endometrial Cancers:

Table (3): Lymph Node Metastasis and Lymph-vascular space invasion (LVSI)distribution according to Risk classification

The probability of having a negative LN Metastasis decreases with FIGO classification. The probability of patient with presence relative to absence LN Metastasis increases with FIGO classification especially in the III and IV classification (Figure 2). So, we can reject the null hypothesis and claim there is evidence of a statistically significant association between LN Metastasis and FIGO classification (χ² (3) = 80.8 Pr = 0.000). Similar pattern is found regarding the association between LN Metastasis and Grade classification (Figure 2). The probability of patient with Metastasis increases with Grade specification (χ² (2) =59 Pr = 0.000).

Figure (2): Distribution of FIGO classification and Tumor Grade within LN Metastasis groups

The logistic regression test the factors that can help to predict if a patient would be in the negative or positive LN Metastasis groups. It generates odds ratio which is a measure of association between a certain factor and LN Metastasis in a population. Specifically, it shows how the presence of each factor has an effect on the presence of LN Metastasis.

Our binary dependent variable is LN Metastasis (0 if absence, 1 if presence). The independent variables are: FIGO classification (I, II, III and IV)^[1]. Grade classification (I, II and III), with classification I as the reference group. Myometrial invasion (0 if <50%, 1 if >50%) and LVSI is 0 if there is no invasion, 1 if there is lymph vascular invasion. Tumor size is 0 for <2cm, 1 for >2cm). Patients with comorbidities such as hypertension and diabetes are categorized as 1 and 0 if there are no comorbidities. Patients with a family history are represented by 1 while patients with no family history are represented by 0.

From the regression result, going up from one level of FIGO to the next multiplies the odds of positive LN Metastasis by 4.95 (p<0.001). For Grade there was no difference between Grade I and Grade II in predicting relative risk of having positive LN Metastasis, however, patients with Grade III classification are 7.12 times more likely to have positive LN Metastasis than those with Grade I classification (p<0.05). Also patients with Myometrial Invasion more than 50% have a 7.12 times the odds of the group with less than 50% Myometrial Invasion of having positive LN Metastasis (p<0.05). The odds are 4.12 times higher that a patient with Lymph vascular invasion will have positive LN Metastasis compared to a patient with no Lymph vascular invasion (p<0.05). The patient group with comorbidities has 2.68 times the odds of the non- comorbidities group of having LN Metastasis (p<0.10). Tumor size and Family history are insignificant; there is no evidence that these factors are associated with positive LN Metastasis (Table 4).

Table (4): Logistic Regression of LN metastasis with group of parameters

Number of observations=  180. LR chi2(8) =112.62. Prob > chi2

Discussion

In this study, we investigated the role of routine use of pelvic systematic lymphadenectomy in the management of all cases uterine cancer. We found that in low-risk patients where tumor grade I-II and FIGOclassification I, only 6.52% of cases had lymph node metastasis, stage I represented 59.4% of all the cases in the study. These patients should not be subjected to comprehensive pelvic lymphadenectomy. Lymphadenectomy can be considered for staging purposes in patients with high risk factors.

Neubauer et al. (2011) discussed that lymphadenectomy as a part of surgical staging is not required in patients assessed intraoperatively to be at low risk for lymph node metastasis (

 Braun (2016) stated that pelvic and para-aortic lymphadenectomy remain controversial. Several studies have noted an associated improvement in survival, whereas others have not. There is no consensus about which patients will require lymph node staging.

Colombo et al. (2016) and Philippe et al. (2016) stated that patients with low risk endometrioid carcinoma (grade 1 or 2 and superficial myometrial invasion <50%) have a low risk of lymph node involvement. Therefore, lymphadenectomy is not recommended for these patients. Patients with intermediate risk (deep myometrial invasion >50% or grade 3 with superficial myometrial invasion <50%), data have not shown a survival benefit of systematic lymphadenectomy. Lymphadenectomy can be considered for staging purposes in these patients. Patients with high risk (grade 3 with deep myometrial invasion >50%), lymphadenectomy should be recommended. Lymphadenectomy to complete staging could be considered in previously incompletely operated high-risk patients to tailor adjuvant therapy.

Concin et al. (2020)suggested pre- and intra-operative work-up by riskgroup allocation on biopsy according to FIGO grading of endometrial carcinoma is required for adequate planning of therapy.Histopathologic grade has prognostic relevance. A modified binary FIGO grading is recommended lumping together grade 1 and grade 2 endometrioid carcinomas as low-grade and grade 3 as high-grade. Use of magnetic resonance imaging (MRI) techniques are highly specific in the assessment of deep myometrial invasion, cervical stromal involvement, and lymph node metastasis.Positron emission tomography (PET) scanning has an excellent specificity for the pre-operative assessment of lymph node metastases in patients with endometrial carcinoma. A pre-operative computerizes tomogram (CT) scan has a clinical utility in patients with endometrial carcinoma in detecting metastatic disease.Frozen section of endometrial biopsy material is obsolete. Myometrial invasion should not be assessed by frozen section.

Raffone et al. (2022) suggested that sentinel lymph node (SLN) biopsy through cervical injection may be routinely adopted instead of systematic pelvic and para-aortic lymphadenectomy in surgical staging for high-risk groups of early-stage endometrial cancer patients, as well as in low-risk groups. Lymphadenectomy carries the risk of increased morbidity, including lymphoedema, lymphocyst formation, and nerve injury. Moreover, it is technically difficult to perform in the obese population, which represents a large proportion of patients with endometrium cancers.

Accorsi et al. (2020) explained that sentinel lymph node (SLN) mapping does not increase morbidity in the surgical treatment of endometrial cancer patients, and compared with comprehensive lymphadenectomy, it has a lower risk of complications. Our findings support the use of the SLN algorithm in endometrial cancerpatients.

  Raffone et al. (2022) stated that sentinel lymph node (SLN) biopsy has shown the potential to significantly reduce the risk of post-operative morbidity and long-term complications. Additionally, it may be associated with a more intensive pathologic assessment (i.e., ultra-staging), with the advantage of detecting low-volume metastasis, which could be missed by standard histological examination SLN biopsy through cervical injection may be routinely adopted instead of systematic pelvic and para-aortic lymphadenectomy in the surgical staging for high-risk groups of early-stage EC patients, as well as in low-risk groups.

The National Comprehensive Cancer Network (NCCN) guidelinesin 2014, approved the sentinel lymph node (SLN) biopsy as an alternative to systematic lymphadenectomy for the staging of apparent uterine-confined endometrial cancers in selected cases.(National Comprehensive Cancer Network®,2021).

Conclusion

         According to results observed in this study, lymph nodeswere involved more in stage III &IV non-endometroid cancers. Systematic lymphadenectomy should not be used routinely in the management of endometrial cancer. It should be replaced by other methods. Use of more precise and less aggressive methods to detect lymph node metastasis such as the use of frozen sections, sentinel lymph nodes during surgical procedures, and molecular markers may be useful to predict preoperatively tumor aggressiveness and lymph node metastasis.

Recommendations

-      Prospective randomized trials have yet assessed the efficacy of sentinel lymph node (SLN) mapping procedures in endometrial cancer, and detection of long-term survival data.

- Recruitment of patients with high grade disease and non-endometrioid endometrial cancers into trials investigating the role of sentinel node surgery in clinical management pathways

-      Molecular markers may be useful to predict preoperatively tumor aggressiveness and lymph node metastasis.

- Histopathologic tumor type and grade in endometrial biopsy is required. Pre-operative mandatory work-up. Thoracic, abdominal, and pelvic CT scan, MRI, ultrasound should be considered to assess ovarian, nodal, peritoneal, and other sites of metastatic disease.

CONFLICT OF INTEREST

           No conflict of interest was declared by the authors.

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دور إستئصال العقد اللمفاوية المنهجي الروتيني في إدارة معالجة سرطان بطانة الرحم: دراسة أترابية بأثر رجعي

بثينة خليل قريو ⁽¹⁾- عواطف محمد بوسهمين⁽²⁾- محمد أحمد بن سعود⁽³⁾-ابتهاج طاهر حسن⁽⁴⁾- سعاد عيسي زايد⁽⁵⁾- مهند طاهر بن طاهر⁽⁶⁾- نهله إبراهيم بيت المال⁽⁷⁾

1- قسم أمراض النساء، الجامعةالدولية الليبية الطبية، بنغازي، ليبيا. 2، 3- قسم العلاج الإشعاعي، المعهد القومي للأورام، مصراتة ليبيا.  4- قسم العلاج الإشعاعي، مستشفى طرابلس الجامعي. 5- قسم العلاج الإشعاعي، المعهد القومي للأورام، صبراتة, ليبيا.

 6- جامعة مصراتة، ليبيا.  7- باحث إحصائي، جامعة غلاسكو كالدونيان، غلاسكو ,المملكة المتحدة

خلفيه البحث: سرطان بطانة الرحم هو خامس أكثر أنواع السرطان شيوعا بين النساء في جميع أنحاء العالم. غالبا ما يكون استئصال العقد اللمفاوية المنهجي الروتيني للغدد الليمفاوية الحوضية جزءا من التدريج الجراحي. ولا يتم هذا الإجراء عالميا. والآثار العلاجية لاستئصال العقد اللمفاوية هي قضية نقاش كبيرو يمكن أن تؤثر مضاعفات استئصال العقد اللمفاوية بما في ذلك الورم اللمفاوي والأكياس اللمفاوية على نوعية جودة حياة المرضى.

الهدف من البحث: تقييم الاستخدام الروتيني لاستئصال العقد اللمفاوية المنهجي في الإدارة السريرية لجميع حالات سرطان بطانة الرحم.

المريضات والأساليب: أجريت دراسة استعادية وصفية بأثر رجعي في ثلاثة معاهد وطنية متعددة المراكز للسرطان (طرابلس ومصراتة وصبراتة) تقع في غرب وشمال ليبيا، في الفترة من يناير 2020 إلى مايو 2022. في الدراسة ،و قد تم تسجيل ما مجموعه 180حالة تم علاجهم من سرطان بطانة الرحم. وكان مقياس النتيجة الأولية هو معدل نقائل العقد الليمفاوية فيما يتعلق بالورم (حجم وعمق غزو بطانة الرحم والدرجة والنتائج النسيجية المرضيةوالانتشار في الفراغ اللمفاوي الوعائي) وخصائص المرضى (العمر- وحالة الحيض-عدد الأولاد- والأمراض المشتركة بما في ذلك السمنة).وتم تقسيم المرضى إلى مجموعتين: أقل من ستين عاما وما فوق الستين، وحالة الطمث فترة ما قبل انقطاع الطمث وبعد انقطاع الطمث،و وجود أولاد أو عدم وجود أولاد،و مؤشر كتلة الجسم السمنة (BMI) أقل من 25 وفوق 25، ووجود أو عدم وجود أمراض مصاحبة.

نتائج البحث:لم يكن هناك ارتباط كبير بينانتقال ورمسرطان الرحم الي العقد الليمفاوية وخصائص المرضى. و كانت هناك ارتباطات كبيرة مع جميع عوامل الورم باستثناء حجم الورمحيث كان مستوى الأهمية أقل من 05.0. بالنسبةلتصنيف سرطان الرحم بتصنيف (FIGO)،مثلت تصنيفالمرحلة الأولى ما يقرب من 60 % من العينة (59.44 %)، والمرحلة الثانية 18.9 %، والمرحلة الثالثة 18.3 %، والمرحلة الرابعة (3.3 %). كان لدى المرضى ذوي المخاطرالمنخفضة(تصنيفFIGOالمرحلة الأولىI، الدرجة 1-2)وقدانتشر المرض السرطاني للغدد الليمفاوية في 6.5% فقط من الحالات،فيالمخاطر المتوسطة FIGO II))المرحلة الثانية،في وجود أي درجة وكان غزو العقد الليمفاوية بنسبة 17.65%، والمخاطر العالية(FIGOIII،FIGO IV)84.84.%، و 100% على التوالي. و كان معدل الإصابة الإجمالي بالانتقالللعقدالليمفاوية في سرطان بطانة الرحم يزداد بشكل متناسب مع الزيادة في الدرجات. (حوالي 9% في الدرجة1،19% في الدرجة2،و76% في الدرجة 3). في حالات غزو سرطان بطانة الرحم لسماكة عضلة الرحمانتقلالورم الخبيث للعقد الليمفاوية في 11% من الحالات مع أقل من 50% غزو سرطان بطانة الرحملعضلة الرحم، مقارنة بحوالي 38% من المرضى الذين يعانون من أكثر من 50% من الغزو العضلي للرحم. النتائج النسيجية المرضية و كان الانتقال للغدد الليمفاوية الاكثر مع الأورام المتباينة بشكل سيئ (64%)، وحدث أقلها مع سرطان بطانة الرحم(endometrioid)(23%). قد أثر الانتشار في الفراغ اللمفاوي الوعائي بشكل كبير على انتقال السرطانللعقد الليمفاوية، وحدث في 15.2% من المجموعة منخفضة الخطورة(FIGOالمرحلة الأولى) وكانت الأعلى (100%) في المجموعة عالية الخطورة(FIGO IV).

الاستنتاج:يجب استبدال استئصال العقد اللمفاوية المنهجي الروتيني بطرق أخرى أكثر دقة وأقل عدوانية مفيدة للتنبوء والكشف عن انتشار الورم الخبيث في العقد الليمفاوية مثل استخدام الأقسام المجمدة والغدد الليمفاويةالخافرة،لرسم خرائط الغدد الليمفاوية الخافرةأثناء العمليات الجراحية.والعلامات الجزيئية والتصوير المقطعي المحوسب)(CTوصور الرنينالمغناطيسي (MRI)، والمسح بالموجات فوق الصوتية)(USSمفيدا للتنبؤ بعدوانية الورم قبل الجراحة.يجب النظر في هذه التحقيقات لتقييم انتشار السرطان للمبيض والعقدي والبروتوني وغيرها من مواقع المرض النقيليالتي تؤثر في خطة العلاج ما بعد الجراحة(استخدامالعلاج الكيماوي والاشعاعي)

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التوصيات: - استخدام التجارب المنضبطة المعشاه لتحديد أهمية إجراء رسم خرائط العقدة الليمفاوية الخافرة في سرطان بطانة الرحم، واستخدامها الكشف عن بيانات البقاء على قيد الحياة على المدى الطويل.

 - قد تكون العلامات الجزيئية مفيدة للتنبؤ بعدوانية الورم قبل الجراحة وتساعد في تحديد انتشار الورم الخبيث في العقدةالليمفاوية.

      - يجبتحديد نوع الورم النسيجي المرضي والدرجة عن طريق خزعة بطانة الرحم كإجراءروتيني قبل الجراحة.

     - يجب النظر في التصوير المقطعي المحوسب للصدر والبطن والحوض والتصوير بالرنين المغناطيسي والموجات فوق الصوتية لتقييم المبيض والعقدي والبروتوني ومواقع أخرى من الأمراض النقيلية.