Fine Needle Aspiration Received: June 24, 2014 Accepted after revision: February 16, 2015 Published online: April 16, 2015
Acta Cytologica 2015;59:149–155 DOI: 10.1159/000380937
Evaluation of Ultrasound-Guided Fine-Needle Aspiration Cytology of Ovarian Masses with Histopathological Correlation Subrata Pal a Srabani Chakrabarti a Debasis Deuoghuria b Jyoti Prakash Phukan a Anuradha Sinha a Prabhat Kr Mondal c
Departments of a Pathology, b Radiodiagnosis, and c Gynaecology and Obstetrics, Bankura Sammilani Medical College, Bankura, India
Key Words Cytohistology · Image-guided fine-needle aspiration cytology · Ovarian cysts · Ovarian tumours · Pre-operative diagnosis · Ultrasound guidance
present study. Diagnostic accuracy was 93.94% in respect to the correct diagnosis. Cytohistological discrepancies and limitations of the study are discussed. Conclusion: US-guided FNAC has proved as a quick, economic and safe procedure in diagnosing ovarian masses with brilliant accuracy. © 2015 S. Karger AG, Basel
© 2015 S. Karger AG, Basel 0001–5547/15/0592–0149$39.50/0 E-Mail [email protected] www.karger.com/acy
Introduction
A large variety of non-neoplastic and neoplastic pathologies may arise from the ovaries. Preoperative pathological evaluation of ovarian mass is always challenging because of the difficulty in gaining access [1]. At present, sampling from intra-abdominal and pelvic lesions is quite easier with the help of ultrasound (US) and computed tomography (CT) [2]. Although histopathology is the gold standard, image-guided fine-needle aspiration cytology (FNAC) is an important step in the diagnosis of abdominal pelvic masses [1, 2]. FNAC is a simple, quick, minimally invasive, relatively inexpensive procedure for the pre-operative diagnosis of ovarian masses [3]. The accuracy of cytodiagnosis can approach that of histopathology when applied by well-trained and experienced practitioners [1]. FNAC under image guidance can be done with the use of US, CT and magnetic resonance imaging (MRI). Ultrasonography (USG) is a rapid, inexpensive and versatile Correspondence to: Dr. Subrata Pal Department of Pathology, Bankura Sammilani Medical College Gobindanagar, PO-Kenduadihi Bankura, West Bengal 722102 (India) E-Mail subratapal1985 @ gmail.com
Downloaded by: Univ. of California San Diego 198.143.33.33 - 8/25/2015 7:02:19 AM
Abstract Background: Preoperative cytodiagnosis of ovarian masses is a difficult process, and sampling of pelvic masses is quite easier after the improvement of imaging techniques. Though histopathology is the gold standard, fine-needle aspiration cytology (FNAC) under ultrasound (US) guidance can be a valuable tool for pre-operative diagnosis of ovarian lesions, especially in the hands of an experienced pathologist. Objective: The present study was performed to evaluate the role of US-guided FNAC in pre-operative cytological diagnosis of ovarian masses in comparison with histopathology, and to assess the pitfalls and limitations of cytological interpretation. Materials and Methods: This study was conducted over a 2-year period on 70 cases of ovarian masses, which were evaluated by US-guided FNAC. Sensitivity, specificity and diagnostic efficacy were calculated using histopathology as gold standard. Results: On cytological evaluation, non-neoplastic cysts, and benign and malignant ovarian tumours were diagnosed in 8, 18 and 40 cases, respectively. On histopathology, 62 cases were concordant with cytology. Sensitivity and specificity were 95.23 and 95.83%, respectively, in the
Color version available online
12 Non-neoplastic 10
Benign Malignant
8 Cases (n)
technique, and the most commonly used imaging procedure in our hospital. Unlike CT, exposure to ionising radiation or contrast material is not needed in USG and it can be repeated easily if required [4]. CT and MRI scans give better ideas about the anatomical details, architecture and nature of the lesions, and also help in the staging of malignant ovarian tumours [1]. A CT scan visualises accurate localisation, with excellent needle visibility during the aspiration procedure. But both CT and MRI are costlier, time-consuming procedures. USG has an added advantage of real-time visualisation of the needle tip during the aspiration procedure, which enables successful aspiration of a lesion [5]. Aspiration cytology can differentiate between neoplastic and non-neoplastic lesions, and between benign and malignant ovarian tumours, and may obviate the need of a diagnostic surgical procedure [6]. Till today, gynaecologists are hesitant to accept the role of FNAC in the diagnosis of ovarian masses because of the controversial opinion about the potential risk of needle tract dissemination. The risk of seeding malignant cells in the abdominal cavity during needle aspiration has been overestimated, and it has no clinical and pathological documentation [2, 7]. US- as well as laparoscopy-guided needle aspiration has become an important tool in the management of functional ovarian cysts in the young [6]. Geier and Strecker [8] have suggested the use of FNAC in the diagnosis of recurrent and metastatic tumours, suspected benign cysts and tumours with unsuitable conditions for laparotomy. FNAC under US guidance can be regarded as the investigation of choice for the diagnosis of ovarian malignancy in early-stage disease as there is a clear association between the tumour stage at diagnosis and prognosis [3]. The present study was taken up with two main objectives: (1) to demonstrate the efficacy of US-guided FNAC in the diagnosis of ovarian masses and (2) to identify the pitfalls and limitations of cytodiagnosis.
6 4 2 0
0–10
11–20
21–30
31–40
41–51
>60
Age (years)
Fig. 1. Bar diagram of the age distribution according to the type of ovarian mass.
cent or distant organs. All patients with proven ovarian lesions were included in the study group only after receiving written consent. Patients with pelvic masses of non-ovarian origin and patients with suspected or known coagulopathy were excluded from the study group. Aspirations were done using 22- to 23-gauge needles with 10-ml disposable syringes. Lumbar puncture needles were utilised for deep-seated lesions. One aspiration was done in most of the cases. Repeat aspirations were done in case of inadequacy of the first aspiration. Smears were fixed in alcohol as well as air dried. Air-dried smears were stained with Leishman-Giemsa stain, May-Grünwald-Giemsa stain and alcohol-fixed smears were stained with Papanicolaou stain. After surgery, all excised specimens of ovarian masses were sent to our histopathology laboratory. All biopsy specimens were undergone successive fixation steps in formalin, processing by standard procedures, embedding in paraffin, section cutting and staining with haematoxylin and eosin.
Results
The present study was conducted in our institute from January 1, 2012, to December 31, 2013. Ethical approval was taken from the institutional ethical committee. The study was conducted on 70 patients, who were subjected to US-guided FNAC of ovarian masses and histopathological examination of the excised ovarian mass after resection. Patients with suspected ovarian masses were selected and referred from gynaecology departments for pre-operative cytological diagnosis. We collected data about history (age, presenting complaints, signs and symptoms) and detailed clinical examination (bilaterality, ascites and signs related to metastasis) in each case. Each patient was evaluated by USG to assess size, consistency, loculation, bilaterality, ascites, and involvement of adja-
150
Acta Cytologica 2015;59:149–155 DOI: 10.1159/000380937
The present study included over 70 cases of ovarian masses. Patients ranged in age from 1.5 to 69 years, with a median age of 32 years and an average age of 33.84 years. The age distribution of the cases is shown in figure 1. Considering the clinical presentations, the most common symptom was an abdominal lump (50 cases, 71.43%). Other common presentations were abdominal pain (46 cases, 65.71%), ascites (27 cases, 37.75%), menstrual irregularity (6 cases, 8.75%) and postmenopausal per-vaginal bleeding (4 cases, 5.71%). All the ovarian tumours with ascites were diagnosed as malignant. Thirteen cases were asymptomatic, and these were incidentally diagnosed by USG during Pal/Chakrabarti/Deuoghuria/Phukan/ Sinha/Mondal
Downloaded by: Univ. of California San Diego 198.143.33.33 - 8/25/2015 7:02:19 AM
Materials and Methods
Non-neoplastic lesions Corpus luteal cyst Endometriotic cyst Luteal cyst
8 3 3 2
(12.12%) (4.54%) (4.54%) (3.03%)
Benign ovarian tumours
18
(27.27%)
Surface epithelial tumours Benign serous cyst Benign mucinous cyst
14 10 4
(21.21%) (15.15%) (6.06%)
Germ cell tumours Benign cystic teratoma Granulosa cell tumour
4 2 2
(6.06%) (3.03%) (3.03%)
Malignant ovarian tumours
40
(60.6%)
Surface epithelial tumours Serous cyst adenocarcinoma Mucinous cyst adenocarcinoma Adenocarcinoma (NOS)
33 19 8 6
(50%) (28.79%) (12.12%) (9.09%)
7 4 1 2
(10.6%) (6.06%) (1.51%) (3.03%)
Malignant germ cell tumours Dysgerminoma Yolk sac tumour NOS
the evaluation of other organs; 52 cases (74.28%) were unilateral and 18 cases (25.72%) had bilateral ovarian involvement. US examination revealed that in 22 cases (31.43%) the ovarian mass was entirely cystic and in 13 cases (18.57%) entirely solid, but in the majority (35 cases, 50%), they were partially solid and partly cystic. US-guided FNAC yielded adequate material in 66 cases; aspirates were inadequate in 4 cases (5.71%). According to cytomorphological features, ovarian masses were classified as nonneoplastic lesions, and benign and malignant tumours. The cytological diagnoses of all the adequate aspirates have been presented in table 1. Among the 8 cytologically diagnosed non-neoplastic cystic lesions, 7 cases were consistent with histopathology. The discordant case was a benign serous cyst which was cytologically interpreted as follicular cyst. On histopathological examination, 16 cases of benign ovarian tumours were consistent with the cytological diagnosis; a discrepancy was seen in 2 cases. A case of cytologically diagnosed serous ovarian cyst and another case of mucinous cyst adenoma proved to be borderline tumours on histopathology (table 2). Forty cases were diagnosed as malignant ovarian tumours, and most of these were malignant surface epithelial tumours (33 cases). We could not categorise 6 malignant surface epithelial tumours using FNAC, and these were diagnosed as adenocarcinoma not otherwise specified (NOS). After US-Guided FNAC of Ovarian Masses
histopathological examination, 3 of them were diagnosed as serous adenocarcinoma. Clear-cell carcinoma, endometrioid adenocarcinoma and metastatic mucinous carcinoma constitute another 3 adenocarcinoma (NOS) cases in histopathology. One cytologically diagnosed serous adenocarcinoma proved to be a borderline tumour on histopathology. The cytodiagnosis of all the cases of malignant germ cell tumours was concordant with the histopathological diagnosis. Among the 2 cases of malignant germ cell tumours (NOS), one was diagnosed as yolk sac tumour and the another was diagnosed as embryonal carcinoma on histopathology. No immediate or late complication has been noted following FNAC, and each case was kept in observation for at least 24 h. On comparison with histopathology, we found 2 false-negative cases and 1 false-positive case in our study group (table 3). In the present study, sensitivity and specificity were 95.23 and 95.83%, respectively, and the diagnostic accuracy of FNAC was 93.94%.
Discussion
Neoplastic and non-neoplastic ovarian masses are very frequent in clinical practice. Several diagnostic methods, e.g. imaging modalities (USG, CT and MRI) and determination of tumour marker levels (like CA-125, CEA and β-hCG), are used for the diagnostic evaluation of ovarian tumours [1]. However, all of them have a limited role in defining the exact nature (benign vs. malignant) of the lesions. Histopathology is considered the gold standard for the diagnosis of ovarian masses, but in recent time, USguided FNAC is used as a rapid, versatile, inexpensive and relatively accurate procedure for the pre-operative diagnosis and management of ovarian masses [1, 2]. In the present study, most of the non-neoplastic and benign ovarian masses were diagnosed in young and child-bearing-age patients. Our findings were consistent with observations of previous workers [1, 2, 8–10]. All of the non-neoplastic lesions were
Acta Cytologica 2015;59:149–155 DOI: 10.1159/000380937
Evaluation of Ultrasound-Guided Fine-Needle Aspiration Cytology of Ovarian Masses with Histopathological Correlation Subrata Pal a Srabani Chakrabarti a Debasis Deuoghuria b Jyoti Prakash Phukan a Anuradha Sinha a Prabhat Kr Mondal c
Departments of a Pathology, b Radiodiagnosis, and c Gynaecology and Obstetrics, Bankura Sammilani Medical College, Bankura, India
Key Words Cytohistology · Image-guided fine-needle aspiration cytology · Ovarian cysts · Ovarian tumours · Pre-operative diagnosis · Ultrasound guidance
present study. Diagnostic accuracy was 93.94% in respect to the correct diagnosis. Cytohistological discrepancies and limitations of the study are discussed. Conclusion: US-guided FNAC has proved as a quick, economic and safe procedure in diagnosing ovarian masses with brilliant accuracy. © 2015 S. Karger AG, Basel
© 2015 S. Karger AG, Basel 0001–5547/15/0592–0149$39.50/0 E-Mail [email protected] www.karger.com/acy
Introduction
A large variety of non-neoplastic and neoplastic pathologies may arise from the ovaries. Preoperative pathological evaluation of ovarian mass is always challenging because of the difficulty in gaining access [1]. At present, sampling from intra-abdominal and pelvic lesions is quite easier with the help of ultrasound (US) and computed tomography (CT) [2]. Although histopathology is the gold standard, image-guided fine-needle aspiration cytology (FNAC) is an important step in the diagnosis of abdominal pelvic masses [1, 2]. FNAC is a simple, quick, minimally invasive, relatively inexpensive procedure for the pre-operative diagnosis of ovarian masses [3]. The accuracy of cytodiagnosis can approach that of histopathology when applied by well-trained and experienced practitioners [1]. FNAC under image guidance can be done with the use of US, CT and magnetic resonance imaging (MRI). Ultrasonography (USG) is a rapid, inexpensive and versatile Correspondence to: Dr. Subrata Pal Department of Pathology, Bankura Sammilani Medical College Gobindanagar, PO-Kenduadihi Bankura, West Bengal 722102 (India) E-Mail subratapal1985 @ gmail.com
Downloaded by: Univ. of California San Diego 198.143.33.33 - 8/25/2015 7:02:19 AM
Abstract Background: Preoperative cytodiagnosis of ovarian masses is a difficult process, and sampling of pelvic masses is quite easier after the improvement of imaging techniques. Though histopathology is the gold standard, fine-needle aspiration cytology (FNAC) under ultrasound (US) guidance can be a valuable tool for pre-operative diagnosis of ovarian lesions, especially in the hands of an experienced pathologist. Objective: The present study was performed to evaluate the role of US-guided FNAC in pre-operative cytological diagnosis of ovarian masses in comparison with histopathology, and to assess the pitfalls and limitations of cytological interpretation. Materials and Methods: This study was conducted over a 2-year period on 70 cases of ovarian masses, which were evaluated by US-guided FNAC. Sensitivity, specificity and diagnostic efficacy were calculated using histopathology as gold standard. Results: On cytological evaluation, non-neoplastic cysts, and benign and malignant ovarian tumours were diagnosed in 8, 18 and 40 cases, respectively. On histopathology, 62 cases were concordant with cytology. Sensitivity and specificity were 95.23 and 95.83%, respectively, in the
Color version available online
12 Non-neoplastic 10
Benign Malignant
8 Cases (n)
technique, and the most commonly used imaging procedure in our hospital. Unlike CT, exposure to ionising radiation or contrast material is not needed in USG and it can be repeated easily if required [4]. CT and MRI scans give better ideas about the anatomical details, architecture and nature of the lesions, and also help in the staging of malignant ovarian tumours [1]. A CT scan visualises accurate localisation, with excellent needle visibility during the aspiration procedure. But both CT and MRI are costlier, time-consuming procedures. USG has an added advantage of real-time visualisation of the needle tip during the aspiration procedure, which enables successful aspiration of a lesion [5]. Aspiration cytology can differentiate between neoplastic and non-neoplastic lesions, and between benign and malignant ovarian tumours, and may obviate the need of a diagnostic surgical procedure [6]. Till today, gynaecologists are hesitant to accept the role of FNAC in the diagnosis of ovarian masses because of the controversial opinion about the potential risk of needle tract dissemination. The risk of seeding malignant cells in the abdominal cavity during needle aspiration has been overestimated, and it has no clinical and pathological documentation [2, 7]. US- as well as laparoscopy-guided needle aspiration has become an important tool in the management of functional ovarian cysts in the young [6]. Geier and Strecker [8] have suggested the use of FNAC in the diagnosis of recurrent and metastatic tumours, suspected benign cysts and tumours with unsuitable conditions for laparotomy. FNAC under US guidance can be regarded as the investigation of choice for the diagnosis of ovarian malignancy in early-stage disease as there is a clear association between the tumour stage at diagnosis and prognosis [3]. The present study was taken up with two main objectives: (1) to demonstrate the efficacy of US-guided FNAC in the diagnosis of ovarian masses and (2) to identify the pitfalls and limitations of cytodiagnosis.
6 4 2 0
0–10
11–20
21–30
31–40
41–51
>60
Age (years)
Fig. 1. Bar diagram of the age distribution according to the type of ovarian mass.
cent or distant organs. All patients with proven ovarian lesions were included in the study group only after receiving written consent. Patients with pelvic masses of non-ovarian origin and patients with suspected or known coagulopathy were excluded from the study group. Aspirations were done using 22- to 23-gauge needles with 10-ml disposable syringes. Lumbar puncture needles were utilised for deep-seated lesions. One aspiration was done in most of the cases. Repeat aspirations were done in case of inadequacy of the first aspiration. Smears were fixed in alcohol as well as air dried. Air-dried smears were stained with Leishman-Giemsa stain, May-Grünwald-Giemsa stain and alcohol-fixed smears were stained with Papanicolaou stain. After surgery, all excised specimens of ovarian masses were sent to our histopathology laboratory. All biopsy specimens were undergone successive fixation steps in formalin, processing by standard procedures, embedding in paraffin, section cutting and staining with haematoxylin and eosin.
Results
The present study was conducted in our institute from January 1, 2012, to December 31, 2013. Ethical approval was taken from the institutional ethical committee. The study was conducted on 70 patients, who were subjected to US-guided FNAC of ovarian masses and histopathological examination of the excised ovarian mass after resection. Patients with suspected ovarian masses were selected and referred from gynaecology departments for pre-operative cytological diagnosis. We collected data about history (age, presenting complaints, signs and symptoms) and detailed clinical examination (bilaterality, ascites and signs related to metastasis) in each case. Each patient was evaluated by USG to assess size, consistency, loculation, bilaterality, ascites, and involvement of adja-
150
Acta Cytologica 2015;59:149–155 DOI: 10.1159/000380937
The present study included over 70 cases of ovarian masses. Patients ranged in age from 1.5 to 69 years, with a median age of 32 years and an average age of 33.84 years. The age distribution of the cases is shown in figure 1. Considering the clinical presentations, the most common symptom was an abdominal lump (50 cases, 71.43%). Other common presentations were abdominal pain (46 cases, 65.71%), ascites (27 cases, 37.75%), menstrual irregularity (6 cases, 8.75%) and postmenopausal per-vaginal bleeding (4 cases, 5.71%). All the ovarian tumours with ascites were diagnosed as malignant. Thirteen cases were asymptomatic, and these were incidentally diagnosed by USG during Pal/Chakrabarti/Deuoghuria/Phukan/ Sinha/Mondal
Downloaded by: Univ. of California San Diego 198.143.33.33 - 8/25/2015 7:02:19 AM
Materials and Methods
Non-neoplastic lesions Corpus luteal cyst Endometriotic cyst Luteal cyst
8 3 3 2
(12.12%) (4.54%) (4.54%) (3.03%)
Benign ovarian tumours
18
(27.27%)
Surface epithelial tumours Benign serous cyst Benign mucinous cyst
14 10 4
(21.21%) (15.15%) (6.06%)
Germ cell tumours Benign cystic teratoma Granulosa cell tumour
4 2 2
(6.06%) (3.03%) (3.03%)
Malignant ovarian tumours
40
(60.6%)
Surface epithelial tumours Serous cyst adenocarcinoma Mucinous cyst adenocarcinoma Adenocarcinoma (NOS)
33 19 8 6
(50%) (28.79%) (12.12%) (9.09%)
7 4 1 2
(10.6%) (6.06%) (1.51%) (3.03%)
Malignant germ cell tumours Dysgerminoma Yolk sac tumour NOS
the evaluation of other organs; 52 cases (74.28%) were unilateral and 18 cases (25.72%) had bilateral ovarian involvement. US examination revealed that in 22 cases (31.43%) the ovarian mass was entirely cystic and in 13 cases (18.57%) entirely solid, but in the majority (35 cases, 50%), they were partially solid and partly cystic. US-guided FNAC yielded adequate material in 66 cases; aspirates were inadequate in 4 cases (5.71%). According to cytomorphological features, ovarian masses were classified as nonneoplastic lesions, and benign and malignant tumours. The cytological diagnoses of all the adequate aspirates have been presented in table 1. Among the 8 cytologically diagnosed non-neoplastic cystic lesions, 7 cases were consistent with histopathology. The discordant case was a benign serous cyst which was cytologically interpreted as follicular cyst. On histopathological examination, 16 cases of benign ovarian tumours were consistent with the cytological diagnosis; a discrepancy was seen in 2 cases. A case of cytologically diagnosed serous ovarian cyst and another case of mucinous cyst adenoma proved to be borderline tumours on histopathology (table 2). Forty cases were diagnosed as malignant ovarian tumours, and most of these were malignant surface epithelial tumours (33 cases). We could not categorise 6 malignant surface epithelial tumours using FNAC, and these were diagnosed as adenocarcinoma not otherwise specified (NOS). After US-Guided FNAC of Ovarian Masses
histopathological examination, 3 of them were diagnosed as serous adenocarcinoma. Clear-cell carcinoma, endometrioid adenocarcinoma and metastatic mucinous carcinoma constitute another 3 adenocarcinoma (NOS) cases in histopathology. One cytologically diagnosed serous adenocarcinoma proved to be a borderline tumour on histopathology. The cytodiagnosis of all the cases of malignant germ cell tumours was concordant with the histopathological diagnosis. Among the 2 cases of malignant germ cell tumours (NOS), one was diagnosed as yolk sac tumour and the another was diagnosed as embryonal carcinoma on histopathology. No immediate or late complication has been noted following FNAC, and each case was kept in observation for at least 24 h. On comparison with histopathology, we found 2 false-negative cases and 1 false-positive case in our study group (table 3). In the present study, sensitivity and specificity were 95.23 and 95.83%, respectively, and the diagnostic accuracy of FNAC was 93.94%.
Discussion
Neoplastic and non-neoplastic ovarian masses are very frequent in clinical practice. Several diagnostic methods, e.g. imaging modalities (USG, CT and MRI) and determination of tumour marker levels (like CA-125, CEA and β-hCG), are used for the diagnostic evaluation of ovarian tumours [1]. However, all of them have a limited role in defining the exact nature (benign vs. malignant) of the lesions. Histopathology is considered the gold standard for the diagnosis of ovarian masses, but in recent time, USguided FNAC is used as a rapid, versatile, inexpensive and relatively accurate procedure for the pre-operative diagnosis and management of ovarian masses [1, 2]. In the present study, most of the non-neoplastic and benign ovarian masses were diagnosed in young and child-bearing-age patients. Our findings were consistent with observations of previous workers [1, 2, 8–10]. All of the non-neoplastic lesions were
