Abstract
Background:
Peritoneal washing (PW) cytology has become a widely accepted procedure for staging of gynecological malignancies.
Aims:
To compare conventional cytology, liquid-based cytology (LBC) and cell block in the evaluation of PWs.
Materials and Methods:
A total of 50 clinically suspected cases of gynecological malignancies were enrolled, which included 41 ovarian neoplasms, eight uterine, and one case of cervical malignancy. The age of the women ranged from 13 to 74 years. The PW samples obtained in all cases were subjected to conventional cytology, LBC, and cell block preparations. Immunohistochemistry (IHC) was applied on cell blocks and analyzed. A comparative evaluation and statistical correlation between the three techniques was performed.
Results:
The number of cases reported as positive for malignancy on conventional smear and LBC were 9 (18%) and 11 (22%), respectively. Fifteen (30%) cases were reported as positive for malignancy on cell block after IHC analysis. All three cytological techniques showed a good correlation in diagnosing peritoneal metastasis on evaluation by Cohen’s kappa score (≤ 1.00). However, the overall sensitivity, specificity, and diagnostic accuracy of PW cytology was 43.8%, 94.4%, and 62%, respectively, taking histopathology as the gold standard. The most common malignancy which led to peritoneal fluid involvement was high-grade serous carcinoma of the ovary.
Conclusion:
The study demonstrates the usefulness of combining the three cytological techniques to diagnose peritoneal metastasis in gynecological malignancies. Cell block with IHC can help in reducing the false-negative cases and further adds to objectivity in ambiguous cases.
Keywords: Cell block, conventional smear, FNA, liquid-based cytology, peritoneal washing
INTRODUCTION
Peritoneal washing (PW) has been a good diagnostic modality to evaluate peritoneal metastasis in gynecological cancers since the early 1950s.[1] This concept was incorporated into the official staging of ovarian cancers by the International Federation of Gynecology and Obstetrics (FIGO) in 1975. Peritoneal spread occurs primarily in ovarian, followed by endometrial cancer.[2] The role of PW in staging ovarian/fallopian tube neoplasms is well established. Although positive PW cytology is no longer included in the staging of endometrial/cervical cancers, still the procedure is carried out for risk stratification of the patients and has prognostic implications.[3] PW cytology identifies any microscopic extent of the tumor in the peritoneal cavity. The comment upon the presence of tumor cells in the PW is of utmost importance as it changes the clinical staging and has a significant impact on the overall prognosis and survival of the patient.[4]
The primary method to assess the PW samples is the evaluation of conventional cytology smears, which has a sensitivity of 42%–51% with high false-negative rates (20%–40%).[5] The increased incidence of nondiagnostic results is primarily attributable to decreased cellularity of the washings. Also, the paucity of cellular elements poses a challenge in distinguishing reactive mesothelial cells from malignant cells. The other factors which add to this include the presence of a hemorrhagic background, formation of thick smears, inadequate fixation, and crushing artifacts.[6]
To overcome these lacunae, liquid-based cytology (LBC) is incorporated, which has a sensitivity of 61%–66% and specificity of 82%–91%, and thus helps lower the error of false-negative reporting.[7,8] This method allows the cytologist to observe uniform cell deposition, which leads to an overall improvement in slide examination and eventually the diagnostic accuracy. The diagnostic sensitivity and specificity of peritoneal wash cytology can be further enhanced by cell block preparations, which imparts better architectural as well as cellular morphology and also increases the yield of malignant cells. In today’s era of precision medicine, there is an increasing role of immunohistochemistry (IHC) and molecular studies in cancer diagnosis. The material from cell blocks can be utilized for these ancillary tests and is a useful diagnostic adjunct.[9]
This study was undertaken with the objective to study the diagnostic utility of cytology in detection of peritoneal metastasis in gynecological malignancies and to further evaluate the efficacy of conventional cytology, LBC, and cell block along with IHC in the PWs. There are very few studies in the literature in which all the three cytological techniques have been evaluated.[7]
MATERIALS AND METHODS
This was a prospective cross-sectional study carried out at a tertiary care hospital, which was approved by the Institutional Ethics Committee (7026/G.M.). A total of 50 clinically and radiologically suspected cases of gynecological malignancies were enrolled. As a part of the routine protocol, in all the cases, the peritoneal cavity was rinsed with 60–100 mL of normal saline as soon as the peritoneum had been incised. The fluid instilled into the cavity was immediately aspirated and sent for cytologic examination.
Cytological examination
The PWs were divided equally into three aliquots for cytological assessment and cell block preparation. The first part for conventional cytology was centrifuged at 2000 rpm for 10 min, the supernatant was discarded, and the deposit was used to prepare three direct smears. Two smears were fixed in 95% alcohol for Papanicolaou (Pap) and hematoxylin & eosin (H&E) staining, and the third air-dried smear was stained with May Grunwald Giemsa. The sediment from the second portion of the washings after centrifugation was suspended into a vial containing 25 mL of CytoRich preservative fluid for LBC using SurePath. After homogenization via vortexing, it was centrifuged to prepare the SurePath preparate. Further processing was done according to the non-gyn protocol of BD SurePath using BD PrepStainTM slide processor to prepare LBC slides and stained with Pap stain. The third portion of the fluid was used for cell block preparation by using the plasma thromboplastin technique. After centrifugation, 100 µL of plasma and 50 µL of thromboplastin were added and mixed well. The clot was processed and embedded in paraffin to obtain a cell block. Multiple sections were cut at 3 µm and stained by H&E stain.[10] Immunocytochemistry was performed on cell block sections in 15 suspicious cases or those positive on conventional smear (CS) and LBC. The immune markers were selected on the basis of the suspected primary tumor and included p53, Ck7, ER, and PR. In addition, WT1 immune staining was done to highlight mesothelial cells.
On CS and LBC smears, cytomorphological features were compared using semi-quantitative scoring based on the cellularity, architectural arrangement, nuclear and cytoplasmic details, and the background. The CS and LBC smears were reported as negative, positive, or suspicious of malignancy. The final cytological diagnosis was rendered after cell block and IHC evaluation as positive or negative for malignancy.
Histopathological examination
Histopathological diagnosis on surgical specimens was taken as the gold standard. Pan hysterectomy specimens along with omentum and peritoneal biopsy were received in 32 cases and salpingo-oophorectomy specimens in 18 cases. The resected specimens were subjected to gross pathological examination and microscopic examination for capsular breech and lymph node metastasis. Sampling of the peritoneum and the omentum was done to detect the presence of tumor metastasis.
The relationship between CS, LBC, and cell block diagnosis was correlated by Cohen’s kappa. The sensitivity, specificity, and diagnostic accuracy of the cell block with IHC was compared with the final histopathological diagnosis.
RESULTS
Out of 50 cases, 41 were of suspected ovarian malignancy, eight of uterine malignancy, and one of cervical carcinoma. The mean age of the patients was 42.28 ± 15.50 years (range = 13–74 years). The majority of the women presented with lower abdominal pain (n = 31, 62%).
Cytological findings
On CS, PW cytology was reported as positive for malignancy in 9 (18%), suspicious for malignancy in 2 (4%), and negative in 39 (78%) cases. On LBC, 11 (22%) cases were positive for malignancy and 3 (6%) were suspicious. On comparing the cytomorphological features on CS and LBC, higher cellularity (2+ to 3+) was seen in 48 (96%) cases on LBC as compared to 38 (76%) on CS with a significant P value (P = 0.0001). The nuclear and cytological details as well as the cleaner background were better appreciated on LBC in comparison to CS [Table 1]. Monolayered sheets of mesothelial cells, papillary fragments, 3D clusters of tumor cells, and psammoma bodies were appreciated better on LBC smears [Figure 1].
Table 1.
Cytomorphological features on CS and LBC (N = 50)
| Cytological feature | CS (no. of cases) | LBC (no. of cases) |
|---|---|---|
| Cellularity (P value 0.0001) | ||
| 0 | 4 | 1 |
| 1+ | 8 | 1 |
| 2+ | 20 | 15 |
| 3+ | 18 | 33 |
| Nuclear and cytoplasmic details (P value 0.018) | ||
| Poor | 5 | 0 |
| Fair | 4 | 1 |
| Good | 41 | 49 |
| Background (P value 0.002) | ||
| Hemorrhagic | 41 | 15 |
| Clean | 9 | 35 |
CS = conventional smear, LBC = liquid-based cytology
Figure 1.
Peritoneal cytology in case of serous carcinoma ovary; (a) conventional smear showing a cluster of tumor cells exhibiting nuclear variability, chromatin clumping, and prominent nucleoli (MGG 400×); (b) liquid-based cytology (LBC) smear showing papillae formation (PAP 400×); (c) LBC smear showing psammoma body (arrow) in the malignant cell cluster (PAP 200×); (d) Cell block (CB) showing a papillary fragment lined with pleomorphic tumor cells (H&E 200×); (e) CB showing diffuse nuclear positivity for p53 in tumor cells (immunohistochemistry [IHC] p53 400×); (f) CB showing cytoplasmic positivity for CK 7 in tumor cells (IHC CK7 200×)
IHC on cell block in suspicious/positive cases was done and showed CK7 (membranous/cytoplasmic) and p53 (diffuse nuclear) positivity in ten cases of serous carcinoma ovary. Nuclear positivity with estrogen receptor and progesterone receptor was seen in one case each of endometrioid carcinoma ovary and endometrial carcinoma. Peritoneal washing was reported as positive for malignancy in two cases of borderline ovarian tumor. One case showed epithelial cells in washings positive for CK7 and negative for p53. The mesothelial cells were highlighted on WT1 stain. Henceforth, after cell block and IHC evaluation, a final diagnosis of positive malignancy was rendered in 15 cases on cytology. A good correlation of 0.81–1.00 between CS, LBC, and cell block technique in the diagnosis of malignancy was observed [Table 2].
Table 2.
Statistical analysis of three cytological techniques (CS, LBC, and cell block)
| LBC | Total | Cohen’s kappa | ||
|---|---|---|---|---|
| Negative | Positive | |||
| CS | ||||
| Negative | 36 (100%) | 3 (21.4%) | 39 (78%) | 0.841 |
| Positive | 0 (0%) | 11 (78.6%) | 11 (22%) | |
| Cellblock | Total | Cohen’s kappa | ||
| Negative | Positive | |||
| CS | ||||
| Negative | 35 (100%) | 4 (26.7%) | 39 (78%) | 0.794 |
| Positive | 0 (0%) | 11(73.3%) | 11 (22%) | |
| LBC | Total | Cohen’s kappa | ||
| Negative | Positive | |||
| Cell block | ||||
| Negative | 35 (100%) | 0 (0.0%) | 35 (70%) | 0.951 |
| Positive | 1 (2.8%) | 14(100%) | 15 (30%) | |
CS = conventional smear, LBC = liquid based cytology
Histopathological findings
On histopathological evaluation, there were 32 malignant and 18 benign cases. The malignant cases were 23 ovarian malignancies, including five cases of borderline histology, eight uterine, and one cervical cancer. Serous carcinoma was the most common histopathological subtype of ovarian cancer (n = 12), and endometrioid adenocarcinoma was the commonest uterine malignancy (n = 6) [Table 3].
Table 3.
Peritoneal washing cytology in various gynecological malignancies
| Histopathological subtype | No. of cases | Positive for malignancy | Negative for malignancy |
|---|---|---|---|
| Ovarian tumors | |||
| Serous carcinoma | 12 | 10 | 2 |
| Endometrioid carcinoma | 3 | 1 | 2 |
| Granulosa cell tumor | 2 | – | 2 |
| Serous borderline tumor | 3 | 1 | 2 |
| Mucinous borderline tumor | 2 | 1 | 1 |
| Immature teratoma | 1 | – | 1 |
| Serous cystadenoma | 11 | 1 | 10 |
| Mucinous cystadenoma | 3 | – | 3 |
| Mature teratoma | 2 | – | 2 |
| Papillary cystadenofibroma | 1 | – | 1 |
| Ovarian leiomyoma | 1 | – | 1 |
| Uterine malignancies | |||
| Endometrioid carcinoma FIGO grade 1 | 3 | 1 | 2 |
| Endometrioid carcinoma FIGO grade 2 | 3 | – | 3 |
| Endometrial stromal sarcoma | 1 | – | 1 |
| Carcinosarcoma | 1 | – | 1 |
| Cervical malignancy | |||
| Cervical adenocarcinoma | 1 | – | 1 |
FIGO = International Federation of Gynecology and Obstetrics
Correlation of cytology with histopathology
The PW cytology was positive in 14 out of 32 malignant cases; which comprised ten serous carcinoma ovary, one ovarian endometrioid adenocarcinoma, and one case each of borderline serous and mucinous ovarian tumors. Among uterine neoplasms, a single case of endometrioid adenocarcinoma showed positive peritoneal cytology [Figure 2]. Out of the eighteen benign lesions, peritoneal cytology was falsely reported as positive for malignancy after cell block and IHC analysis in one case of serous cystadenoma [Table 3]. The ovarian tumors with borderline histology and positive peritoneal cytology (two out of five) were not upstaged according to the FIGO guidelines and were considered as peritoneal implants. The omentum/peritoneal biopsies showed evidence of metastasis in only seven out of 14 cytology-positive cases. No significant correlation (P = 0.388) was observed between PW cytology and omental/peritoneal biopsy. The diagnostic concordance of cell block findings with final histopathological diagnosis was assessed [Table 4]. The overall diagnostic accuracy was 62%, while the sensitivity and specificity were 43.8% and 94.4%, respectively.
Figure 2.
Peritoneal washings in a case of endometrioid adenocarcinoma; (a) conventional smear reported as negative showed less cellularity of benign mesothelial cells (MGG 200×); (b) liquid-based cytology showing a cluster of tumor cells with prominent nucleoli and intracytoplasmic vacoulation (PAP 400×); (c) Cell block (CB) showing clusters of tumor cells exhibiting nuclear pleomorphism (H&E 400×), (d) CB showing nuclear positivity for ER in tumor cells (immunohistochemistry ER 200×)
Table 4.
Diagnostic concordance of CS, LBC, and cell block with histopathology diagnosis
| Histopathology diagnosis | ||||||
|---|---|---|---|---|---|---|
| Benign | Malignant | Total | ||||
| Diagnosis on CS | ||||||
| Negative | 18 | 100.0% | 21 | 65.6% | 39 | 78.0% |
| Positive | 0 | 0.0% | 11 | 34.4% | 11 | 22.0% |
| Total | 18 | 100.0% | 32 | 100.0% | 50 | 100.0% |
| Diagnosis on LBC | ||||||
| Negative | 18 | 100.0% | 18 | 56.3% | 36 | 72.0% |
| Positive | 0 | 0.0% | 14 | 43.8% | 14 | 28.0% |
| Total | 18 | 100.0% | 32 | 100.0% | 50 | 100.0% |
| Diagnosis on the cell block | ||||||
| Negative | 17 | 94.4% | 18 | 56.3% | 35 | 70.0% |
| Positive | 1 | 5.6% | 14 | 43.8% | 15 | 30.0% |
| Total | 18 | 100.0% | 32 | 100.0% | 50 | 100.0% |
| Final cytology diagnosis | ||||||
| Negative | 17 | 94.4% | 18 | 56.3% | 35 | 70.0% |
| Positive | 1 | 5.6% | 14 | 43.8% | 15 | 30.0% |
| Total | 18 | 100.0% | 32 | 100.0% | 50 | 100.0% |
CS = conventional smear, LBC = liquid-based cytology
DISCUSSION
The detection of metastasis in PW signifies the spread of disease beyond the primary organ of origin and is associated with considerable therapeutic and prognostic implications.[11] Histopathological examination of the peritoneal surface and omentum has been considered the gold standard for staging of gynaecological tumors. PW cytology being cost-effective and less time-consuming with a comparable yield is fairly valuable in the detection of peritoneal metastasis.[12] PW provides wider sampling of the peritoneum and can even detect occult peritoneal disease and hence is considered a sensitive indicator. In many institutions, PW cytology analysis is performed in cases of presumed benign diseases also as it serves as a helpful adjunct in cases with high clinical and radiological suspicion of malignancy.[13] The present study compared the efficacy of PW cytology using conventional cytology, LBC, and cell block with IHC in detection of peritoneal metastasis.
In the current study, the diagnostic yield of LBC for detection of peritoneal metastasis was better as compared to conventional cytology. Cytomorphological details of individual cells were also more pronounced with the LBC technique, as observed in many previous studies.[12,13,14,15,16] Cell block prepared from PWs was useful in all positive cases including the ones with suspicion of malignancy on CS/LBC. The cell block findings in conjunction with IHC confirmed positive PW cytology in 24% of cases in the present study. In a study by Amiri et al.[7] cell block findings confirmed positive PWs for malignancy in 33.3% of cases.
In addition, in today’s era of precision medicine, IHC on cell blocks not only increases the diagnostic accuracy but also helps determine the primary site of malignancy in case of body fluids. This not only promotes rapid diagnosis and early treatment but also obviates the need for biopsy, especially in critically ill patients. A study done by Bansal et al.[17] diagnosed 77.3% of malignant ascitic/peritoneal fluids in a study of 53 cases after cell block and IHC result interpretation. Furthermore, based on clinical details and morphological evaluation, a panel of IHC markers on cell blocks were assessed to ascertain the primary site of malignancy. Cell block is also beneficial in cases with paucity of abnormal cells as it provides a satisfactory cellular yield with a preserved architectural pattern of the tumor.[18,19,20] However, a study done by Mulvany[21] observed the cell block technique to be less sensitive than smear examination in detection of peritoneal metastasis. In their study, 97% of cytologic smears and only 51% of cell blocks prepared from PW showed malignant cells. The possible explanation could be differences in the technique of cell block preparation, leading to isolation of few malignant cells, artifactual cell distortion, or inadequate sections for histopathology. Also, in their study, IHC was not used on cell blocks to differentiate reactive mesothelial cells from malignant cells.
Among all three cytological techniques performed on PW samples, cell block in conjunction with IHC helped in comprehensive evaluation of the cytology for upstaging of the tumor. Overall, a good correlation was observed between conventional and LBC (kappa score 0.841) and between conventional cytology and cell block (kappa score 0.749). A perfect correlation was also observed between LBC and cell block (kappa 0.951), similar to other studies.[7] Positive PW cytology increases the FIGO staging of ovarian carcinoma from IA/IB or IIA/IIB to IC or IIC. Histopathologic examination of peritoneal surfaces and omentum has been considered the gold-standard approach for staging of ovarian carcinoma. However, only seven out of fourteen cytology-positive cases showed omental/peritoneal metastasis on histopathological examination in our study because PW provides a broader sampling of the peritoneum than the random staging biopsies.[20]
Peritoneal lesions in borderline neoplasms are classified as invasive and noninvasive implants, based on the histopathological examination. The combination of cytoarchitectural and nuclear features may help in suspecting these implants on PW cytology, although not possible to further categorize them.[22] Two cases of borderline ovarian tumors in the current study showed positive peritoneal fluid cytology, but were not upstaged. However, in another similar study, the borderline ovarian tumors were upstaged after positive peritoneal cytology.[23] Henceforth, more studies are required to assess the prognostic significance of positive PW cytology in borderline tumors. Also, the positive PWs on cell block in a case of serous cystadenoma could be more likely due to endosalpingiosis or microscopic implant and thus should be interpreted cautiously.
Taking histopathology as the gold standard, the sensitivity of detecting peritoneal metastasis by cytological evaluation in our study was 43.8% and the specificity was 94.4% with an overall diagnostic accuracy of 62%. The results are comparable to those of previous studies that have yielded a diagnostic accuracy of 68%–72%.[12,18] However, a few studies have shown slightly lower diagnostic rates (22%–34%) of PW cytology in detection of peritoneal metastasis.[19,20] The refinement of pathologic staging through the cytologic examination of PW specimens can alter the subsequent recommendation for radiotherapy or chemotherapy.
In conclusion, cell block along with IHC helps overcome the drawbacks associated with each of the techniques individually, thus increasing the diagnostic accuracy and reducing the percentage of false-negative diagnoses. However, studies of larger sample size are required to ascertain the combined usage of these cytological techniques in peritoneal fluid cytology.
Data availability statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Ethical policy and Institutional Review Board statement
The PWs were done as a diagnostic procedure after proper consent of the patient.
Conflicts of interest
There are no conflicts of interest.
Funding Statement
Nil.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.