Introduction
Serous
fluids from the pleural, peritoneal, and
pericardial cavities constitute majority of the
non-gynaecological samples being submitted to any
cytology laboratory. [1] They reflect a wide array
of aetiologies such as infection, injury/trauma,
mechanical obstruction, metabolic diseases, and
malignancy. [2] Around 10% to 25% of these
effusions are caused by malignancy. [3]
Serous effusions
usually are the first clinical manifestation of
malignancy and cytology not only detects
malignancy but is also useful in determining the
primary site of origin, staging, recurrence status
and prognosis of the tumors. [4,5] It is a cost
effective, minimally invasive, simple and safe
procedure which when used in conjunction with
ancillary techniques such as cell block, flow
cytometry, immunocytochemistry and molecular
analysis provides a definitive diagnosis and has a
profound impact on the clinical management. [3]
The sensitivity of cytomorphological evaluation of
malignant effusions ranges from 40% to 97% and the
specificity ranges from 90% to 100%. [2,3] The
diagnostic efficacy of effusion cytology is varied
for reasons such as sample volume, cell content,
different collection/preparation techniques in
different laboratories, overlap between benign and
malignant entities and the experience of the
cytopathologist. Until now, there was no
standardized reporting system for fluid cytology
that could strictly define the diagnostic
terminologies and establish standards for the
sample adequacy to improve interobserver agreement
and communication, influencing further management
based on the risk of malignancy (ROM) assessment
for each category. [5,6]
Hence, The
International System of Reporting Serous Fluid
Cytopathology (TIS) has been developed in
collaboration with the International Academy of
Cytology (IAC) and American Society of
Cytopathology (ASC) to address these issues and
provide a consistent and tiered reporting for
these specimens. The five proposed diagnostic
categories are Non-Diagnostic (ND), Negative for
Malignancy (NFM), Atypia of Undetermined
Significance (AUS), Suspicious for Malignancy
(SFM) and Malignant (MAL) – primary and secondary.
[7]
Currently, only a
few studies have been done based on the above
proposed new system. Therefore, the present study
was conducted with the aim to reclassify serous
fluids into the categories as per TIS, estimate
the risk of malignancy for each category and
determine the diagnostic efficacy of serous fluid
cytology when TIS was applied.
Materials and Methods:
The approval for
conducting the study was obtained from the
institutional ethical committee and the number is
19/2021 dated 20/01/2021 board. This was a
cross-sectional study conducted over a duration of
two years from 1st April 2021 up to 30th
March 2023. The procedures followed were in
accordance with the ethical standards of the
responsible committee on human experimentation
(institutional or regional) and with the Helsinki
Declaration of 1975, as revised in 2000. Purposive
sampling technique was followed. The study sample
included all pleural, pericardial, or peritoneal
effusion samples submitted to the cytopathology
department during the study period. The exclusion
criteria included those slides that were returned
to the patients and slides that were broken and
unavailable for reviewing. Total 235 cases were
included in the study.Complete clinical data were
recorded. The fluid was centrifuged and slides
from the sediment were prepared.
Haematoxylin-eosin, Pap and Giemsa staining was
done.
Slides of all the
cases were reviewed by two experienced
cytopathologist (AK and SM) with more than 10
years) experience. All the cases were classified
as per The International System of Reporting
Serous Fluid Cytopathology (TIS) into one of the
following categories. Non-Diagnostic (ND),
Negative for Malignancy (NFM), Atypia of
Undetermined Significance (AUS), Suspicious for
Malignancy (SFM) and Malignant (MAL) – primary and
secondary. [7]
Final diagnosis was
confirmed by follow-up, clinical history,
radiology, and cell block in 74 cases.
Risk of malignancy
was calculated for individual diagnostic category.
The sensitivity, specificity, positive predictive
value, and negative predictive value depicting the
diagnostic efficacy of TIS were calculated under
three circumstances. In first case, malignant
cases were considered as positives, while SFM and
AUS were taken as negatives. In second case,
malignant and SFM cases were considered positives
while AUS were taken as negatives. Lastly,
malignant, SFM and AUS cases were considered as
positives.
Statistics:
Continuous variables
were expressed as mean and standard deviation.
Categorical variables were expressed as
percentages and proportions. Sensitivity,
specificity, positive predictive value, and
negative predictive value were determined to
assess the diagnostic efficacy of TIS for fluid
cytology. Microsoft excel was used for data
compilation and analysis.
Results
Demographics
and general characteristics of fluid:
In the present
study, a total of 235 fluid aspirates were
included. Final confirmatory diagnosis was
obtained in 74 cases based on thorough clinical
history, cell block or radiological findings. Out
of the total 235 cases, maximum cases were from
the peritoneal cavity 127 (54.04%), followed by
pleural cavity 108 (45.95%). There was no case of
pericardial fluid. Mean age of presentation was 54
± 2.5 years. Male to female ratio was 1.97:1.
Quantity of fluid sent to the cytopathology ranged
from 5 ml to 20 ml. In maximum number of cases,
fluid was clear or straw coloured 167 (71.06%)
followed by blood-tinged fluid in 50 cases
(21.27%). Fluid was turbid in 15 cases (6.38%),
and milky in 3 cases (1.28%). Demographics and
general characteristics of fluid is shown in Table
1.
Table 1: Demographics and general
characteristics of all the cases
|
Type of fluid
|
Pleural fluid
|
Peritoneal fluid
|
No of cases
|
108
|
127
|
Mean age (Years)
|
56.5±11
|
51.5±4.2
|
Gender (no. of cases)
|
Male
|
74
|
81
|
Female
|
34
|
46
|
Male to Female Ratio
|
2.18:1
|
1.76:1
|
Appearance of fluid
|
Clear/Straw
|
68
|
99
|
Blood tinged
|
30
|
20
|
Milky
|
2
|
1
|
Turbid/Pus
|
8
|
7
|
Volume
|
5 to 10 ml
|
107
|
123
|
10 to 20 ml
|
1
|
4
|
Cyto-diagnostic
categories:
Out of a total of
235 cases of fluid examined, distribution of cases
in the diagnostic categories were as follows, 11
(4.6%) in non-diagnostic (ND), 208 (88.51%) in
negative for malignancy (NFM) (Figure 1), 5
(2.12%) in atypia of undetermined significance
(AUS) (Figure 2), 2 (0.85%) in suspicious for
malignancy (SFM) (Figure 3) and 9 (3.82%) in
malignant (MAL) category (Figure 4). (Table 2)
|
Figure 1: A: Sediment smears
showed only neutrophils. Acute
inflammatory process. B: Shows only
lymphocytes. CBNAAT was negative. A and B:
Negative for malignancy. (Hematoxylin and
Eosin, × 400) |
|
|
Figure
2: Atypical cell in an acute inflammatory
background. -Atypia of undetermined
significance. (Hematoxylin and Eosin, ×
400) |
Figure
3: Atypical cell clusters in an acute
inflammatory background- Suspicious for
malignancy. (Hematoxylin and Eosin, × 400) |
|
Figure
4: A: Tumor cells forming 3D balls in
malignant effusion. B: Two populations of
cells suggestive of malignancy. C: Cell
block from pleural fluid showing signet
ring cells of adenocarcinoma stomach.
(Hematoxylin and Eosin, × 400) |
Table 2: Distribution of cases in
individual diagnostic categories as per
TIS
|
Cytodiagnostic categories
|
Cytology
No of cases (%)
|
Confirmatory cases
No of cases (%)
|
1
|
11 (4.6%)
|
3 (4.05%)
|
2
|
208 (88.51%)
|
55 (74.32%)
|
3
|
5 (2.12%)
|
5 (6.75%)
|
4
|
2 (0.85%)
|
2 (2.70%)
|
5
|
9 (3.82%)
|
9 (12.16%)
|
|
235
|
74
|
Predominant
cell pattern in benign and malignant cases:
Among 208 cases in
whom benign diagnosis was made, maximum cases
showed lymphocyte predominance (140/208, 67.3%).
Only neutrophils (30/208, 14.4%) and mesothelial
cells (5/208, 2.4%) were also noted. Rest of the
cases showed mixed pattern of cells. Malignancy
was detected most commonly in pleural fluid. All
the positive cases in pleural fluid were
metastatic, with the most common site of primary
being from lung followed by breast carcinoma. In
peritoneal fluid, metastasis from gastrointestinal
tract tumours were seen. Site wise distribution of
malignant cases and predominant non-cancerous cell
pattern in each case is depicted in Table 3.
Table 3: Shows the distribution of
primary site of the malignant cases, the
involved site and the predominant cells
present in the fluid
|
Case No
|
Site of primary
|
Site of effusion
|
Predominant cell type
|
Associated cells
|
1
|
Breast -infiltrating ductal carcinoma
|
Pleural
|
Malignant cells
|
Lymphocytes and Mesothelial cells
|
2
|
Lung- Adenocarcinoma
|
Pleural
|
Neutrophils
|
Lymphocytes and malignant cells
|
3
|
Gastrointestinal-Adenocarcinoma
|
Peritoneal
|
Malignant and mesothelial cells
|
Lymphocytes
|
4
|
Lung-Squamous cell carcinoma
|
Pleural
|
Malignant cells
|
Mixed inflammatory cells
|
5
|
Breast - infiltrating ductal carcinoma
|
Pleural
|
Malignant cells
|
-
|
6
|
Lung-Squamous cell carcinoma
|
Pleural
|
Malignant cells
|
Mesothelial cells
|
7
|
Lung - Adenocarcinoma
|
Pleural
|
Reactive mesothelial cells, Malignant
cells
|
Mixed inflammatory cells
|
8
|
Lung -Adenocarcinoma
|
Pleural
|
Mesothelial cells, Malignant cells
|
Mixed inflammatory cells
|
9
|
Lung -Adenocarcinoma
|
Pleural
|
Malignant cells
|
Mesothelial cells and mixed inflammatory
cells
|
Correlation
between cytology and final diagnosis:
Correlation between
cytology and final diagnosis was performed on the
basis of histopathology, clinical history or
radiology findings.(Table 4) Final diagnosis could
be affirmed in 74 cases (3.18%). Concordance
between cytology and final diagnosis was obtained
in 71 cases whilst discordant diagnosis was
obtained in three cases. All the three cases in
which discordant diagnosis was made were placed in
the atypical category of TIS. Amongst these three
discordant diagnoses, two were false positive and
one was a case of false negative diagnosis.
Table 4: Shows correlation between
cytology and final diagnosis in 74 cases
|
Category
|
Cytology
|
Confirmatory diagnosis
|
|
|
Consistent
|
Non consistent
|
1
|
11 (4.6%)
|
3
|
3 (Benign)
|
-
|
2
|
208 (88.51%)
|
55
|
55
|
-
|
3
|
5 (2.12%)
|
5
|
02
|
03 – 2 Benign (FP), 1 Malignant (FN)
|
4
|
2(0.85%)
|
2
|
2
|
-
|
5
|
9(3.82%)
|
9
|
9
|
|
Total
|
235
|
74
|
71
|
|
FP-False positive, FN-False negative
|
Diagnostic
efficacy:
The sensitivity,
specificity, positive predictive value, and
negative predictive value under various
circumstances is shown in Table 5. We calculated
the values depicting the diagnostic efficacy of
TIS under three circumstances. In first case,
malignant cases were considered as positives,
while SFM and AUS were taken as negatives. In
second case, malignant and SFM cases were
considered positives while AUS were taken as
negatives. Lastly, malignant, SFM and AUS cases
were considered as positives. In all the
scenarios, the sensitivity and specificity was
high.
Table 5: Sensitivity, Specificity,
Positive Predictive Value, and Negative
Predictive Value under various
circumstances
|
|
A
|
B
|
C
|
Sensitivity
|
100
|
91.67
|
92.85
|
Specificity
|
94.82
|
100
|
96.5
|
Positive Predictive Value
|
75
|
100
|
86.67
|
Negative Predictive Value
|
100
|
98.21
|
98.21
|
In A – Malignant cases were considered as
positives, while SFM and AUS were taken as
negatives. In B – Malignant and SFM cases
were considered positives while AUS were
taken as negatives and in C - Malignant,
SFM and AUS cases were considered as
positives.
|
Risk of
malignancy in individual diagnostic categories:
Risk of malignancy
was obtained for each category by dividing the
number of cases diagnosed as malignant by the
total number of cases in that category. Risk of
malignancy was 100% each in SFM and malignant
categories and 40% in AUS category.
Table 6: Shows risk of malignancy in
individual category of TIS
|
Category
|
ROM
|
1
|
0
|
2
|
0
|
3
|
40
|
4
|
100
|
5
|
100
|
Discussion
Serous fluids offer
rich cytopathological as well as molecular
information on benign and malignant conditions.
Being a simple, cost-effective, and minimally
invasive diagnostic tool, it seems timely that a
unified approach to reporting these specimens has
been proposed. [3,8] The International System for
Reporting Serous Fluid Cytopathology (ISRFC)
consists of 5 categories namely – non-diagnostic
(ND), negative for malignancy (NFM), atypia of
undetermined significance (AUS), suspicious of
malignancy (SFM) and malignant (MAL). [8]
The present study
was a retrospective, cross sectional analysis of
235 pleural and peritoneal samples based on the
“The International System for Reporting Serous
Fluid Cytopathology (ISRFC)”, recategorizing them
into the five categories and calculating the
diagnostic accuracy and ROM for each category.
Overall, most of the specimens were peritoneal
samples (54.04%, n = 127) with a mean age of 51
years.
Non-Diagnostic
(ND)
The ND category
includes those specimens that are acellular or
nearly acellular, without atypia, compromised by
degeneration, poor preservation, obscuring blood,
etc. making them uninterpretable. Eleven of the
235 cases (4.6%) were reclassified to this
category. Confirmatory diagnosis was available for
3 of the 11 cases and all 3 were concordant.
Therefore, it is recommended that enough specimen
is collected (75ml) for accurate reporting. [8]
However, in this study, volume of sample ranged
from 5-20ml with maximum number of specimens
falling in the 5-10ml range.
Negative for
Malignancy (NFM)
208 cases fell into
the NFM category as they contained only benign or
reactive cellular components with no
morphological, phenotypic, or molecular evidence
of mesothelial or non-mesothelial malignancy.
Concordance between cytology and final diagnoses
was obtained in 55 of the cases.
Atypic of
Undetermined Significance (AUS)
In the present
study, in AUS category, 5 cases were indeterminate
for mesothelial and non-mesothelial malignancy and
contained cells (macrophages, mesothelial cells,
or cells from cytologically bland malignant
tumors) of uncertain nature, either because of
qualitative or quantitative factors. 2 of the 5
cases were concordant while the rest were
discordant. Amongst these 3 discordant diagnoses,
2 were false positive and one was a case of false
negative diagnosis. The false-positive rate
reported in literature is 0.1-1%. [11,12] The low
cellularity, measurement errors, screening errors
and failure to recognise cytopathological features
could explain these findings. [9] The ROM was 40%
which is in consensus with ROM in various
literatures ranging from 20-70% with an average of
45%. [2,3,5-7,10,11]
Suspicious
for Malignancy (SFM)
The suspicious for
malignancy category includes specimens showing
cytologic features usually found in malignant
lesions but insufficient either in quality or
quantity for a definitive diagnosis of malignancy
and 2 concordant cases were assigned this
category. The ROM was 100% which is higher than
most of the literature ranging from 57-88%.
[2,3,5-7,10,11] The lack of standardized
diagnostic criteria thus far and an intrinsic bias
of knowing patients’ history could be potential
reasons for the difference in ROM values.[2,11]
Malignancy
(M)
A total of 9 out of
235 cases (3.82%) were categorized into the
malignant category as the specimens included those
with definitive findings and/or supportive studies
indicating mesothelial or non-mesothelial
malignancies. This percentage reported in lower
than that reported in literature which ranges from
10.4-20.5%. [12] This may be attributed to the
small sample size and lack of ancillary testing.
All nine cases were concordant on final diagnoses.
Eight of the 9 cases
(88.89%) were pleural fluids malignancies with the
primary being predominantly lungs (75%) followed
by breast (25%). Previous reports show that
pleural fluid malignancies account for 10-30% only
and of these 50-70% are due to lung, breast, and
ovarian cancer, as well as lymphoma. [13,14] This
discrepancy between the results of present study
and previous reports could be due to different
selection criteria, study methodology and
ancillary techniques employed. The peritoneal
fluid malignancy was from a primary
gastrointestinal adenocarcinoma which has been
reported as the most common cause of malignant
ascites in both sexes. [15] Literature has shown
that ROM for this category ranges from 89-100%
with a mean ROM of 99% (±0.1%). [11] In this
study, ROM for this category was 100%.
Taking only
malignant cases as positive, Lobo et. al., in
their study of 1496 pleural effusion samples and
763 peritoneal effusion samples had a sensitivity
of 61.4%. specificity of 100%, PPV of 100% and NPV
of 71.7%. [3] Another study by Pinto D et. al,
showed similar results with 52.21% sensitivity,
100% specificity, 100% PPV and 76.28 NPV. [5] In
the present study, although the specificity
closely matched their results, the sensitivity and
NPV were 100% and PPV for 75%. These results
support the role of cyto-analysis in confirming
malignancy. The comparison of diagnostic efficacy
of TIS with that of the existing literature is
shown in Table 7.
Table 7: Shows comparison of diagnostic
efficacy of TIS in the present study with
that reported in the literature
|
|
Lobo et al*
|
Pinto D et al
|
Song et al
|
Hou et al
|
Pinto D et al
|
Pergaris et al
|
Present Study
|
Sensitivity
|
A
|
61.4
|
|
|
|
52.21
|
|
100
|
B
|
66.5
|
|
|
|
60.29
|
77.95
|
91.67
|
C
|
67.9
|
|
|
|
62.50
|
|
92.85
|
Specificity
|
A
|
100
|
|
|
|
100
|
|
94.82
|
B
|
98.95
|
|
|
|
98.56
|
99.5
|
100
|
C
|
97.95
|
|
|
|
96.65
|
|
96.5
|
PPV
|
A
|
100
|
|
|
|
100
|
|
75
|
B
|
98.45
|
|
|
|
96.47
|
98.625
|
100
|
C
|
97.1
|
|
|
|
92.39
|
|
86.67
|
NPV
|
|
|
|
|
|
|
|
A
|
71.7
|
|
|
|
76.28
|
|
100
|
B
|
74.25
|
|
|
|
79.23
|
91.6
|
98.21
|
C
|
74.85
|
|
|
|
79.84
|
|
98.21
|
ROM
|
1
|
78.55
|
17.4±8.9
|
|
|
40
|
8.33
|
0
|
2
|
25.1
|
21±0.3
|
3.7
|
|
20.16
|
7.15
|
0
|
3
|
56.25
|
66±10.6
|
20.9
|
39
|
42.86
|
35.89
|
40
|
4
|
83.95
|
82±4.8
|
57.1
|
64
|
78.57
|
88.33
|
100
|
5
|
100
|
99±0.1
|
89.3
|
|
100
|
100
|
100
|
* Taking only statistics for peritoneal
and pleural samples only
|
Considering
malignant and suspicious for malignancy cases as
positives and AUS as negatives, the present study
showed a sensitivity of 91.67%, specificity of
100%, PPV of 100% and NPV of 98.21%. This was in
stark contrast to the findings of other similar
studies having sensitivity values ranging from
60-67% and NPV ranging 74-79%. [3,7] However, a
study by Pergaris et. al. involving 1028 cases in
total showed similar specificity, PPV and NPV of
99.5%, 98.62% and 91.6% respectively. [6]
If malignant,
suspicious for malignancy and AUS are considered
as positives, the present study showed a higher
sensitivity value of 92.85%, a higher NPV value of
98.21% and a lower PPV of 86.67% compared to Lobo
et. al. and Pinto D et. al. [3,5]
Comparison of
diagnostic efficacy of TIS in the present study
with that reported in the literature is depicted
in Table 7.
Limitations
In this study, all
samples evaluated were conventional preparations.
Many studies have reported higher accuracy with
liquid-based preparations, despite some
controversy. [16] The absence of pericardial
samples reflects the clinical management of the
situation. The criteria for drainage are strict
and patients presenting with malignant pericardial
effusion often present with concomitant malignant
pleural effusion which is easier to tap. Follow-up
confirmatory diagnosis was not available for
majority of the cases.
It is a known fact
that the combination of clinicopathological
findings as well as immunocytochemistry play a
crucial role in diagnosis of malignant serous
effusions. Immunocytochemistry aside, serous
effusions also serve as an ideal material for
molecular analysis. [17,18] Due to technical
limitations, ancillary studies were not possible
in our set-up. These techniques would have allowed
to reassign more cases to malignant category and
identify the primary.
The IRSSF will
eliminate many inconsistencies in reporting
effusions and the nonspecific terms such as
“suggestive of”, “suspicious for” etc, thereby
providing a common language for all
cytopathologists, clinicians, and institutions to
be utilised in patient management.
Conclusion:
ISRSFC is easy to apply and has high diagnostic
efficacy. Most of the serous effusions fall in
negative for malignancy category. Mesothelial
cells are not important for specimen adequacy.
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