Introduction:
Abnormal uterine bleeding (AUB) is a common cause of consultation in gynecology outpatient department. [1] It is caused by a wide variety of functional and organic causes and it is one of the commonest complaints requiring endometrial sampling. [2]
Dilatation and curettage (D & C) has been used as a traditional method and is considered gold standard for evaluation of AUB. However, complications like side effects of anesthesia, pain, perforation along with economic burden and need for hospitalization are major limitations of D & C. [3-4] In this era of modern medicine, wherein there exist an inclination to provide an out-patient care with minimum discomfort to the patient, there is a need for a test which can counterfeit all these drawbacks. Endometrial aspiration cytology (EAC) is one such method. Since its introduction in 1950 several instruments have been designed and tested like endometrial brush, Gravlees' jet wash, Mendhosa cannula,Isaacs endometrial sampler, Mi -Mark cannula, endopap sampler, MR syringe, nasogastric tube and intracath cannula. [4]
Use of nasogastric tube for aspiration renders this procedure a quick, safe and cost-effective test. [5] Several centers around the globe have been using endometrial aspiration cytology on regular basis and have recorded a high diagnostic accuracy in determining the endometrial status. [6-8] However, in India, its use is limited mainly to research and there are few studies describing its role in evaluating AUB.
The present study was planned in view of the necessity for simple and rapid cytological techniques for diagnosing endometrial lesions and to assess its efficacy by histopathological correlation.
Methodology
The present study was a cross-sectional study conducted in the departments of Pathology and Gynecology, at a tertiary care hospital. The sample size was based on purposive, convenient sampling technique. All the consecutive cases presenting with AUB to the obstetrics and gynecology department during the study period were included in the study. Pregnant women and patients having systemic bleeding disorders, acute pelvic inflammatory disease, in-situ intra-uterine contraceptive device were excluded from the study.
Detailed history, general examination, systemic examination and local examination findings were recorded in the excel sheet. After explaining details of the procedure, a written informed consent was obtained from the patient prior to the procedure and also for the publication for research purposes. Ethical clearance certificate was obtained from the institutional ethical committee.
Under absolute aseptic conditions, endometrial aspiration sample was collected by using nasogastric tube in the minor operation theater. No anesthesia was used during the procedure. Material thus obtained was expelled onto clean non greasy glass slides and direct smears were prepared by spreading the material with another clean glass slide. Slides were then air dried or fixed in absolute alcohol. Air-dried smears were stained by May-Grunwald Giemsa and alcohol fixed smears were stained with Hematoxylin and eosin stains. This was followed by dilatation and curettage and material obtained was gently blotted on a gauze piece to remove excess blood and serial imprints were obtained by pressing the material firmly for 3-5 seconds on clean glass slides. Smears were immediately fixed in absolute alcohol or air- dried. Smears were stained by May-Grunwald Giemsa stain or Hematoxylin and eosin stain like direct smears. The endometrial biopsy was then sent for histopathological examination. Stained slides were reported by two experienced cytopathologist with 10 years of experience and final diagnosis was based on consensus among them.
All the EAC smears were classified into 5 categories based on the principles mentioned by Yanoh et al with minor modifications.[9] These categories were benign, hyperplasia, suspicious of malignancy, malignancy and inadequate
Statistical analysis: Data was expressed as mean and standard deviation, proportions and confidence intervals. Diagnostic efficacy of EAC was determined by calculating sensitivity, specificity, positive predictive value and negative predictive value with histopathology as gold standard.
Results
In the present study, total 127 cases underwent EAC and D & C. Youngest patient was 20 years and the oldest was 70 years. Mean age was 41.57 ± 8.42 years. Majority of patients belonged to 31 to 40 years of age group. Of the cases, 51.9% belonged to reproductive age group, 35.4% were perimenopausal and 12.5% were in the menopausal age group.
Out of total 127 cases, menorrhagia was the most common pattern of abnormal uterine bleeding seen in 46 cases (36.2%) cases, followed by polymenorrhoea in 41 cases (32.3%), metromenorrhagia in 22 cases (17.3%) and oligomenorrhoea in 18 cases (14.2%).
All the 127 cases were classified into five categories as benign, hyperplasia, suspicious of malignancy, malignancy and inadequate
Out of total 127 cases of endometrial aspiration cytology (EAC), benign diagnosis was rendered in 107 cases (84.2 %). Hyperplasia was reported in 11 cases (8.6%) with 10 cases (7.9%) of simple hyperplasia and one (0.8%) case of atypical hyperplasia. Malignancy was reported in two cases (1.6%). Inadequate smears were seen in seven cases (5.5%) on endometrial aspiration cytology.
| Table 1: Distribution according to various cytodiagnostic categories by endometrial aspiration cytology and histopathology |
| Diagnostic categories |
Endometrial aspiration cytology |
Histopathology |
Benign |
107 (84.2%) |
102 (80.3%) |
Hyperplasia |
11 (8.6%) |
13 (10.2%) |
Suspicious of malignancy |
00 |
01 (0.7%) |
Malignancy |
2 (1.5%) |
3 (2.3%) |
Inadequate |
7 (5.5%) |
8 (6.2%) |
Total |
127 |
127 |
Out of 107 cases in benign category 57 (44.9%) were in proliferative phase, 48 (37.8%) in secretory phase and two cases showed endometritis. Out of 57 cases diagnosed as proliferative phase on endometrial aspiration cytology. Diagnosis of proliferative phase was obtained at histopathology in 47 cases. In the remaining ten cases of discordant diagnosis, five cases were inadequate on histopathology. Out of remaining five cases diagnosed as proliferative phase in endometrial aspiration cytology, two cases were diagnosed as simple hyperplasia. one case each diagnosed as secretory phase, endometrial adenocarcinoma and disordered proliferative endometrium subsequently at histopathology.
Out of 48 cases of secretory phase diagnosed on endometrial aspiration cytology, concordant diagnosis was obtained in 46 cases. There was one case each of polyp and simple hyperplasia on histopathology which was wrongly diagnosed as secretory phase on endometrial cytology. Endometritis was diagnosed in two cases which was confirmed on histopathology.
Simple hyperplasia was diagnosed in ten cases on aspiration cytology. All ten Cases showed similar diagnosis on histopathology. However, two cases one of each proliferative phase and secretory phase on cytology turnout to be simple hyperplasia on histopathology. Hence 12 cases of simple hyperplasia diagnosed at histopathology in the present study.
There was one case of complex hyperplasia which was underdiagnosed as simple hyperplasia at cytology.
There was no case reported as suspicious for malignancy on EAC. However, there was one case reported as suspicious for malignancy on histopathology. There were two case of adenocarcinoma on aspiration cytology which showed concordant at histopathology. However, there was one case of adenocarcinoma reported at histopathology which as misdiagnosed as proliferative phase on cytology. There were seven (5.5%) cases reported as inadequate on EAC.
For statistical analysis, we first excluded cases which were inadequate on histopathology. Then the inadequate cases on endometrial cytology were excluded. By this procedure we excluded total 17 cases which were inadequate on histopathology, aspiration cytology. Hence, we had 110 cases which were further subjected to statistical analysis.
Table 2 shows correlation of endometrial aspiration cytology and histopathology in 110 cases.
| Table 2: Correlation of endometrial aspiration cytology and histopathology in 110 cases |
| |
Endometrial Aspiration Cytology |
|
| (Concordant diagnosis) (%) |
(Discordant diagnosis) (%) |
Biopsy |
Proliferative phase |
42 (38.1%) |
-- |
42(38.1%) |
Secretory phase |
45 (40.9%) |
2 (1.8%) |
47(42.7%) |
Endometritis |
2 (1.8%) |
|
2(1.8%) |
Disordered proliferative endometrium |
-- |
1(0.9%) |
1(0.9%) |
Polyp |
-- |
1(0.9 %) |
1(0.9%) |
Simple hyperplasia |
9 (8.1%) |
3 (2.7%) |
12(10.9%) |
Complex hyperplasia |
|
1(0.9%) |
1(0.9%) |
Suspicious of malignancy |
0 |
1(0.9%) |
1(0.9%) |
Malignancy |
2 (1.8%) |
1 (0.9%) |
3(2.7%) |
Total |
100 |
10 |
110 (100%) |
Table3 shows diagnostic accuracy of EAC with histopathology as gold standard
| Table 3: Sensitivity, specificity, positive predictive value, negative predictive of endometrial aspiration Cytology in various categories |
|
Proliferative phase |
Secretary phase |
Hyperplasia |
Malignancy |
Variable |
Value |
95% CI |
Value |
95% CI |
Value |
95% CI |
Value |
95% CI |
Sensitivity |
100% |
91.59-100 |
95.74% |
85.46- 99.48 |
75% |
42.81-94.51 |
66.67% |
9.43- 99.16 |
Specificity |
91.18% |
81.18 - 96.69 |
96.83% |
89-99.61 |
98.98% |
94.45-99.97 |
100% |
96.61-100 |
Positive predictive value |
87.50% |
76.53 - 93.76 |
95.74% |
85.18-98.88 |
90% |
55.48-98.48 |
100% |
- |
Negative predictive Value |
100% |
|
96.83% |
88.70-99.16 |
97% |
92.39-98.85 |
99.07% |
98.5-99.81 |
| CI=confidence interval |
 |
Figure 1 A: EAC smears from proliferative phase endometrium showing tubules of uniform width. Inset shows streaming. (Haematoxylin & Eosin x 40)
Figure 1 B: EAC smears from secretary phase with abundant cytoplasm. Inset show columnarization (Haematoxylin & Eosin x 100) |
 |
Figure 2 A: EAC smears from simple hyperplasia showing extensive cellularity. (Haematoxylin & Eosin x 40)
Figure 2B: EAC smears from complex hyperplasia showing cribriform pattern. (Haematoxylin & Eosin x 40) |
 |
Figure 3: EAC smears from endometrial adenocarcinoma showing irregular protrusion pattern (a), papillary pattern (b), bare nuclei (c) and nuclear atypia (d) (Haematoxylin & Eosin x 100) |
Discussion
Endometrial carcinoma is now one of the most common cancer of female genital tract with highest mortality rate, next only to ovarian cancer. Detection of endometrial carcinoma at an early stage when patients are usually asymptomatic and hence amenable to cure is the need of the time, where in diagnostic EAC has a major role to play. It is quite evident that the interest in the use of EAC has not reached the level as for the use of cytology in other organs. Though several studies have well established the accuracy of EAC as a diagnostic modality in endometrial pathology, endometrial cytology is an area feared by morphological pathologist. [5]. The main reason being two-fold, one is the difficulty in obtaining adequate sample and the other being the difficulty in interpretation as well as distinction of abnormal from normal endometrial cells.
Menstrual disorders vary with the age and an increase in the incidence of AUB has been associated with increase in age. In the present study, maximum number of cases who presented with AUB belonged to 3rd decade of life. This was similar to the findings of Sandeepa et al. [10] However majority of the studies report a slightly higher age group for AUB. In our study, second commonest group affected was 41-50 years encompassing 35.4 % of all the cases. This was similar to 33.5% reported by Jairajpuri et al. [2] Mean age of presentation in our study was 41.57± 8.42 years which was similar to Agarwal et al. [11] Dadhania et al reported a lower mean age of 36.5 years. [12] Rise in the incidence of early menopause (<40 years) may be the cause of increased cases of AUB in a decade earlier in the present study, as compared to that reported in various other studies. Similarly, women in reproductive age group commonly encounter hormonal imbalance leading to functional bleeding, as was seen in present study. An increase in the incidence of AUB with age is attributed to the decreasing estrogen levels due to anovulation and increase resistance to gonadotropins. [12]
In the present study, menorrhagia was the most common pattern of AUB accounting for 36.2 % of cases followed by polymenorrhagia in 32.3 % of cases. This was in accordance with the findings of 41% and 41.7% by Jairajpuri et al and Katuwal et al respectively, but lower than 51.9 % as mentioned by Muzzaffar et al.[ 2, 13,14]
Cytological evaluation of endometrium has been used by few hospitals since 1980. Japan, after the introduction of health insurance law for the elderly in 1987, has been using endometrial aspiration cytology (EAC) with good results. Diagnostic criteria for the identification of cyclic, hyperplastic, pre-malignant and malignant conditions were laid down in initial days and emphasis was given to the nuclear size and shape variability, including morphometry. However, this did not sustain the bias of subjectivity. Later Skaarland et al proposed diagnostic criteria based on architecture and growth pattern of large tissue fragments. [15] In 2009 Yanoh et al introduced a new system for reporting EAC which incorporated together qualitative as well as quantitative elements, analogous to that used in Bethesda system for reporting cervical cytology. In the present study, categorical classification of various entities was done according to that of Yanoh et al. [9]
Inadequacy rates reported in the literature for EAC varies from 1.6% to 27%, depending on the technique used. [16,17] In our study, inadequacy rate was 4.7%.
In the present study, out of total 127 cases, cyclic endometrium was reported in 105 (82.6%) of cases, with 57 (54.2%) in proliferative phase and 48 (45.7%) in secretory phase. Our findings were fairly comparable to Reena et al.[18] This was slightly higher than that reported by Nelson et al in 27.2% and 21.5% respectively. [19] In the present study, cytohistological concordance was 100% for proliferative phase.
Normal proliferative phase endometrial smears show large tissue fragments with tubular lumen with in it. Stromal cells are attached to the periphery. Streaming effects seen in stromal cells is a significant finding in smears from proliferative phase endometrium. [20] (Figure 1 A) Caution in not interpreting variations in nuclear size among different fragments as atypia would avoid false negative diagnosis. Background examination is of utmost importance with only bare nuclei and stromal cells or red blood cells favoring a diagnosis of normal cyclical endometrium.
Secretory endometrium does not differ much in the architecture from proliferative phase, whilst the composition of cell varies. The cells show cytoplasmic vacuolization indicating of progesterone effect which is more distinct in Giemsa stain. (Figure 1 B) Though it may seem easy, findings are not classical and at times error occur. In the present study, out of 47 cases of secretory phase, two cases were mistakenly classified as proliferative phase at EAC. Jadhav et al in their study, misclassified two cases of secretory phase as proliferative phase due to absence of cytoplasmic vacuoles in endometrial cells. Difficulty lies even in distinguishing endometrial cells from stromal cells. Stromal cells may occur in singles with spindle configuration. When they occur in cluster, the nuclei are seen protruding out from the fragment. [20]
In the present study there was one case (0.8%) of disordered proliferative endometrium on histopathology which was wrongly diagnosed as proliferative phase on EAC. However, this discrepancy did not affect patient management. Nevertheless, disordered proliferative endometrial smears show fragments of endometrial glands and condensed clusters of stromal cells. These changes may mimic endometrial hyperplasia. A precise assessment of cytoarchitectural pattern., cellularity and fragment of cell clumps paves way to accurate diagnosis. [15]
In the present study, endometritis was represented among 1.6% cases. Both the cases had history of intrauterine device insertion. Our findings were consistent with 2% and 1.2% as reported by Sadia et al and Lee et al respectively. [21,22] However higher incidence, reaching up to 24% has been reported. [23] Another non-neoplastic benign pathology which was erroneously diagnosed, was a single case of polyp (0.8%) which was misinterpreted as proliferative phase on EAC.
Jairajpuri et al reported 1.7% cases of polyp. [2] Lack of specific criteria at EAC for diagnosing polyp often leads to error. Polyp at D & C is identified by presence of thick walled blood vessels along with papillary endometrial fragments. The endometrial glands within the polyp are dissimilar from the adjacent endometrial glands.
Yanoh et al established certain objective criteria for diagnosing endometrial hyperplasia.[9] Endometrial hyperplasia should be suspected when the number of abnormal clumps noted in smear are more than 10 and the ratio of abnormal clump to total clump ratio is more than 10%. Earlier authors have used the findings of excessive cellularity, presence of irregular branching, dilated sheets, presence of irregular protrusion and papillary pattern in diagnosing endometrial hyperplasia. Absence of adherence of stromal cells to endometrial fragments is also considered as an important clue. [15]
The prevalence of simple hyperplasia without atypia in present study was 9.0% (Figure 2 A). This was in accordance with Nelson et al, who reported simple hyperplasia without atypia in 7.2 % cases. [19] Various studies mention a wide range of incidence for endometrial hyperplasia ranging from 6.6% to 25 %.[24-26]
In the present study, out of 12 cases of simple hyperplasia on histopathology, accurate diagnosis was possible only in nine cases at cytology. This was mainly due to low cellular yield. Jhadav et al reported similar pitfall leading to under diagnosis of two cases of simple hyperplasia as proliferative phase in their study. [20] The third case was over diagnosed as complex hyperplasia without atypia at EAC. The difficulty in distinguishing simple hyperplasia from complex hyperplasia without atypia is inherent to cytology but has important therapeutic implications. Schimizu et al emphasized the importance of quantitative assessment of cell clump and ability to identify the clumps as normal as well as abnormal in precisely identifying endometrial hyperplasia at endometrial aspiration cytology. [27]
Complex hyperplasia without atypia was recorded in one case (0.9 %) at histopathology which was misinterpreted as simple hyperplasia without atypia at cytology (Figure 2 B). Accuracy of EAC in diagnosis of complex hyperplasia is variable. Earlier reports claim a higher rate of accuracy. [10] However, similar to the present study, pitfalls were observed by Meisels et al, who could diagnose hyperplasia in only 50 % of cases. [28] Complex hyperplasia with or without atypia connotes a premalignant process and mandates a biopsy confirmation. Much of the confusion in limitation regarding the diagnosis of complex hyperplasia at cytology is related to overlapping features of simple hyperplasia at one end and adenocarcinoma at another end. The sole finding of cohesive sheets of endometrial cells with enlarged nucleoli favor a diagnosis of atypical hyperplasia [5].
Diagnosis of suspicious for malignancy is rendered when the specimen meets all the architecture and cytological features of malignancy but lack the characteristics tumor diathesis. In the present study, one case of suspicious of malignancy was diagnosed at histopathology which was under reported as complex hyperplasia with atypia at EAC. A cytological diagnosis of atypical endometrial hyperplasia or suspicious malignancy should prompt for a similar work up, both requiring endometrial curettage for a final diagnosis.
The accuracy of cytology in diagnosis of malignancy in AUB has been documented by Schachter et al and Jhadav et al. [20,29] Utility of EAC in screening of asymptomatic women has been investigated in several studies and has gained importance in recent years. Some studies claim higher accuracy rate for detection of endometrial carcinoma by EAC as compared to D & C. However, some studies reveal lower accuracy rate. In the present study, out of three cases of adenocarcinoma diagnosed at histopathology, two cases showed concordant diagnosis at EAC (Figure 3). There was one false negative diagnosis in which under diagnosis of proliferative phase was made at EAC. Malignant smears show papillary, tubulopapillary, fimbriated fragments with fibrous connective tissue stroma. The architecture is disorganized with prominent cytologic atypia. Importance of background in diagnosis of malignancy cannot be overemphasized. False negative diagnosis is a cause of concern. False positive diagnosis occurs in presence of reactive atypia in endometritis and dark staining nuclei. Findings of some studies advocate the use of EAC as a screening tool for post-menopausal bleeding and at-risk women. Nevertheless, asymptomatic women or those who have minimal symptoms may harbor occult endometrial adenocarcinoma and hence are more suitable candidates for cytology. Early detection of these primary has significant impact on survival rate. Our study enjoyed a high diagnostic accuracy. Comparison of diagnostic accuracy of EAC in detecting various endometrial patterns in various studies and present study is depicted in Table 4.
| Table 4: Shows comparison of diagnostic accuracy of endometrial aspiration cytology among various other studies with present study |
|
Baxi et al[8] |
Schachter et al[29] |
Present study |
Proliferative phase |
100% |
86.4 % |
100 % |
Secretory phase |
87.5% |
78.5% |
95.74 % |
Simple hyperplasia |
60 % |
77% |
75 % |
Endometrial carcinoma |
100% |
100% |
66.67 % |
Sensitivity and specificity of EAC in various studies range from 81% to 96% and 83% to 96% respectively.[1,18,20] In the present study, we observed a slightly lower rate of sensitivity for EAC in diagnosing of malignancy. This was mainly due to the difficulty in obtaining enough material in one case of adenocarcinoma which was underreported as proliferative phase at EAC. Similarly, difficulty in typing hyperplasia lead to the slight decrease in diagnostic accuracy.
With the increase in the incidence of endometrial carcinoma in the west and anticipating a similar surge in this part of the world it is important to screen both symptomatic women presenting with AUB as well as asymptomatic women to detect carcinomas at an early stage. Since EAC is a simple, safe, cost effective tool which can be used as an ambulatory procedure in diagnosing various endometrial lesions, we recommend its use in routine clinical practice. However, further large-scale studies focusing on the usefulness of EAC as a screening tool for endometrial malignancy in asymptomatic women are needed.
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