Article in press - uncorrected proof
J Lab Med 2008;32(6):418–424
2008 by Walter de Gruyter • Berlin • New York. DOI 10.1515/JLM.2008.058
Hämatologie
Cytology of body cavity effusions
Zytologie der Körperhöhlenergüsse
Marianne Engels*
Krankenhaus Düren, Klinik für Hämatologie und
Internistische Onkologie, Klinisch-zytologisches Labor,
Düren, Germany
Abstract
Body cavity effusions are symptoms of different dis-
eases. The microscopic examination of effusion fluid is a
technically simple method, which in many cases may
facilitate further diagnostic workup. In selected cases, a
definitive diagnosis can be established.
Keywords: body cavity; cytology; effusion; morphology.
Zusammenfassung
Körperhöhlenergüsse sind Symptome unterschiedlicher
Grunderkrankungen. Die mikroskopische Untersuchung
von Ergussflüssigkeit ist eine technisch wenig aufwen-
dige, aber sehr aussagekräftige Methode, die in vielen
Fällen eine diagnostische Weichenstellung und in Einzel-
fällen eine definitive Diagnose ermöglicht.
Schlüsselwörter: Erguss; Körperhöhle; Morphologie;
Zytologie.
Introduction
The present paper does not attempt to outline the entire
spectrum of diagnostic procedures for evaluating body
cavity effusions. Rather, it describes the cytomorphology
of cells in serous effusions and its diagnostic relevance.
Other recent review articles deal with further laboratory
methods to examine serous effusions w1–3x.
Pleural effusions, ascites and pericardial effusions
present accumulations of fluid in preformed body cavi-
ties. The surfaces of the right and left pleural cavity, the
abdominal cavity, the pericardial cavity and the organs
*Correspondence: Dr. med. Marianne Engels, Krankenhaus
Düren, Klinik für Hämatologie und Internistische Onkologie,
Klinisch-zytologisches Labor, Roonstr. 30, 52351 Düren,
Germany
Tel.: q49-2421-301864
Fax: q49-2421-307702
E-Mail: marianne.engels@krankenhaus-dueren.de
2008/58
Redaktion: C.T. Nebe
located within the body cavities are covered by a thin
membrane called serosa. The two leaflets of visceral and
parietal serosa are physiologically separated by a thin
layer of lubricating fluid of low protein content with
scarce mesothelial cells and lymphocytes. However, in
the case of increased filtration pressure, e.g., in conges-
tive heart failure, or reduced intravascular osmotic pres-
sure an increased amount of fluid is filtered into the body
cavity. Associated with inflammation, infarction or malig-
nant conditions, damage to the capillary walls usually
occurs and fluid rich in protein and inflammatory cells
may accumulate within the body cavity. Such an effusion
induces a proliferation of the epithelial layer covering the
inner surface of the body cavity, the mesothelium. With-
out a proliferating stimulus mesothelial cells grow in sin-
gle layer. The mesothelium may proliferate extensively
and desquamate large numbers of cells into the effusion.
In benign effusions all cells may be found which occur in
peripheral blood, including the entire spectrum of stim-
ulated lymphatic cells and plasma cells as well as mast
cells and macrophages. Furthermore, in nearly every
benign effusion desquamated mesothelial cells are
found. All other cells are foreign; they are either dislo-
cated by the procedure of thoracentesis or paracentesis
(e.g., squamous epithelium of the skin, striated muscle
of the thoracic or abdominal wall, liver cells), or mixed up
by fistula or perforation (e.g., squamous epithelium in the
presence of fistula or rupture of the esophagus), or the
cells are malignant originating from carcinomatous infil-
tration or metastatic involvement of the body cavity
w4–7x.
Material and methods
For microscopic examination stained slides of cell-
enriched samples are required. There are different meth-
ods of concentrating cells of which the following are
most widely used: a) centrifuge for 10 min at 2000 rpm
(550–600=g), remove supernatant with a pipette, centri-
fuge again for 10 min at 2000 rpm (550–600=g), remove
supernatant and prepare smears of the sediment. This
method of preparation is preferred by our laboratory; b)
preparation using a cytocentrifuge; and c) preparation
using an automatic monolayer device w8–11x.
The routine staining method most widely used in Ger-
many is the May-Grünwald-Giemsa stain (MGG) and is
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Figure 1 Normal mesothelial cells. Left: 100=, MGG. Right: 100=, Papanicolaou stain.
well known from hematology. This stain may be applied
to preparations of effusion fluid without modification. As
a second routine stain, the Papanicolaou stain may con-
tribute valuable information, but it requires wet-fixed
slides placed immediately after spreading the sediment
onto the slide into an alcoholic fixative. Depending on the
clinical problem, special stains, e.g., Prussian blue, lipid
stain, periodic acid Schiff, or immunocytochemistry may
be employed. Furthermore, fluorescence in situ hybridi-
zation (FISH), DNA cytometry and other molecular biol-
ogy techniques may be applied to samples of effusion
fluid. These special methods are not addressed in detail
in this review and readers are referred to the literature
w12–18x.
For any cytologic examination of stained slides a
microscope equipped with transmission light and bright
field is needed, with 10= ocular lenses and 10= and
40= objectives as a minimum. For positive recognition
of small cells and evaluation of details, 63= or 100=
objectives are recommended. In any case of effusion flu-
id several slides should be completely screened using
10= objective lens so as not to miss any malignant cells
which occur only scarcely. Abnormal cells should be
examined using higher magnification and should be
marked for further observation.
Morphology
Benign mesothelial cells have round to oval nuclei with
even, granular chromatin. In many nuclei a round, often
prominent nucleolus is visible. The cytoplasm may be
quite narrow and staining basophilic using MGG, but may
also be rather wide staining bright, often with many small
vacuoles or one single, very large vacuole. Mesothelial
cells may appear as isolated cells or in clusters of vari-
able sizes. The clusters can be single-layered or multi-
Engels: Body cavity effusions 419
layered and often are rosette-like or spherical with a
regular configuration of the cells w4–7, 19x (Figure 1).
The most important questions in evaluating effusion
fluids are the following:
1. Are there indications of an acute serious illness, such
as empyema, fistula, or perforation?
2. Are malignant cells present? If so, is it possible to
classify them safely to a certain type of tumor and to
establish the organ of origin?
If neither empyema nor malignant cells are found, the
different cell populations observed in the sample should
be described.
An empyema or a putride inflammation of the perito-
neum leads to an effusion with a high amount of neutro-
philic leukocytes, a few macrophages and, only some-
times visible, bacteria or other microorganisms. Meso-
thelial cells are found only rarely in empyema. The neu-
trophilic leukocytes often are altered by degeneration. In
cases of fistula or perforation in addition to putride
inflammation there are foreign epithelia, e.g., squamous
epithelium of esophagus or trachea, and sometimes food
particles (Figure 2).
Benign effusions of unspecific origin may contain very
different types of cells in each single case. Often there is
a varied picture with lymphocytes, stimulated lymphatic
cells and many mesothelial cells. Mesothelial cells may
form large clusters. Often a prominent nucleous is visible
w4, 6, 7, 19, 20x (Table 1).
In other cases lymphatic cells predominate, often with
many stimulated lymphatic cells and plasma cells. Such
effusions may occur para- or postpneumonic w21, 22x. In
some cases, a positive differential diagnosis between a
malignant lymphoma, e.g., a lymphoplasmacytic lympho-
ma or a marginal zone lymphoma, and a benign effusion
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420 Engels: Body cavity effusions

Figure 2 Empyema with squamous epithelium from esophagus in esophageal perforation, 40=, MGG (left). Benign effusion with
lymphocytic preponderance, mesothelial cell at center, 100=, MGG (right).

Table 1 Common causes of benign body cavity effusion.

Pleural effusion Ascites Pericardial effusion

Congestive heart failure Liver cirrhosis Congestive heart failure

nephrotic syndrome, uremia nephrotic syndrome, uremia nephrotic syndrome, uremia

Pneumonia, tuberculosis, Pneumonia, tuberculosis, lung Peri- and myocarditis

lung infarction, cholecystitis, infarction, cholecystitis, pneumonia, tuberculosis, lung
pancreatitis pancreatitis, hepatitis infarction

Empyema Putride ascites, Empyema

Collagen diseases, Collagen diseases Collagen diseases,

Dressler syndrome, Dressler syndrome,
postpericardiotomy postpericardiotomy
syndrome syndrome

is impossible without applying further immunologic meth-
ods (Figure 2).
Some cases of benign effusion contain large numbers
of monocytes and macrophages. In cases of long-stand-
ing effusions with hemorrhage, erythrophagocytosis may
be encountered.
Many benign effusions contain increased numbers of
eosinophilic and basophilic leukocytes. Especially large
numbers of eosinophilic leukocytes are observed when
effusions are sampled for a second or third time or in
postoperative effusions.
Long-standing effusions without inflammatory stimulus
may contain only small numbers of cells. Sometimes in
the background cholesterin crystals are visible as an indi-
cation to a long-standing cellular decay.
When one evaluates effusions which correspond to the
different representations described above, one should
always be aware of the fact that as a reaction to carci-
noma the same reactive pattern may be observed. In a
cellular effusion of benign appearance some scarce
malignant cells may be present, which should be detect-
ed by screening several slides of the same sample.
The most common cause of malignant effusion is
involvement of serosal membrane by metastatic or infil-
trative growth of a carcinoma. Secondly, malignant effu-
sion occurs with malignant lymphoma. Effusion by
malignant mesothelioma is increasing in frequency, but
is still much rarer than carcinoma or lymphoma w6, 7, 19,
23x (Table 2).
How are cells of a carcinoma detected? In a benign
effusion there is only one type of cells appearing in clus-
ters, i.e., desquamated mesothelial cells of the serosal
membrane covering the body cavity. All other epithelia
observed in samples of effusion fluid which cannot be
classified as mesothelial cells are suspicious for malig-
nancy. Rare exceptions relate to the above-mentioned
dislocated cells of the wall of the thorax, abdomen or
liver cells. Hence, if a second type of cells forming clus-
ters or solid structures is found in an effusion which is
clearly not of mesothelial origin, this second type of cells
is highly suspicious for carcinoma w6, 7, 19, 23, 24x.
The most common carcinoma in malignant effusion is
adenocarcinoma which may originate from different pri-
maries into all body cavities. Cells of an adenocarcinoma
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Engels: Body cavity effusions 421

Table 2 Common causes of malignant body cavity effusion.

Pleural effusion Ascites Pericardial effusion

Lung cancer, breast cancer, Gastric cancer, pancreatic cancer, Lung cancer, breast cancer,
gastric cancer, pancreatic cancer of gallbladder and bile ducts, gastric cancer, etc.
cancer, etc. ovarian cancer, colorectal cancer, etc.

Malignant lymphoma Malignant lymphoma Malignant lymphoma

Pleural mesothelioma (rare: peritoneal mesothelioma) (rare: pericardial mesothelioma)

usually have enlarged hyperchromatic nuclei which may
clearly be differentiated from the nuclei of neighboring
mesothelial cells. In many but not in all cases a centrally
located macronucleolus is observed. The cytoplasm may
be of variable width and structure depending on the type
of tumor. Often a vacuole of mucin is found intracellularly.
Adenocarcinoma originates from glandular tissue and
mimics glandular structures: single-layered formations of
tumor cells which look similar to ductal epithelium of
glands, acinar formations of tumor cells which resemble
secreting portions of glands, and carcinoma cells pro-
ducing mucin. In addition to clusters of carcinoma cells,
also single cells are observed in many types of adeno-
carcinoma. The primary tumor in most instances cannot
be determined only by cytomorphology. Immunocyto-
chemistry may provide valuable additional information
w14, 25–28x (Figure 3).
Small cell anaplastic carcinoma of the lung presents a
very typical representation in effusion: immature cells of
blastic appearance are observed, displaying a chromatin
structure which resembles the chromatin of blasts of
acute leukemia or high grade lymphoma. The tumor cells
are shed in small, dense clusters. In many cases, nuclei
of tumor cells are molding each other. Blasts of acute
leukemia or high grade lymphoma on the other hand are
always shed as isolated cells (Figure 3).
Squamous cell carcinoma only rarely produces malig-
nant effusion. In most of these cases, an involvement of
the serosa by direct infiltration of the tumor is found. Ker-
atinized tumor cells stain intensely blue in MGG stain,
non-keratinized tumor cells of a squamous cell carcino-
ma cannot be distinguished from cells of a poorly differ-
entiated adenocarcinoma w29x.
High grade lymphoma can easily be recognized in effu-
sion. Immature cells of blastic appearance are found
which are shed as isolated cells. Depending on the sub-
type of lymphoma the blasts may be of different size.
They also may have a different chromatin structure, num-
ber and size of nucleoli as well as a cytoplasm of varying
width and staining properties. Burkitt lymphoma shows
a very typical appearance: the blasts are of middle size
with a monotonous representation, often with many
small, clear vacuoles of cytoplasm. Mitoses, degenerat-
ing blasts and macrophages are found in abundance.
While in middle-Europe an infiltration of peritoneum is
common in Burkitt lymphoma, involvement of pleura is
much rarer. Suspected Burkitt lymphoma is a diagnostic
emergency requiring urgent confirmation or exclusion. It

Figure 3 Malignant effusion due to ovarian cancer, tumor cells in the right, normal mesothelium at the left, 40=, MGG (left). Small
cell anaplastic lung cancer, 100=, MGG (right).
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422 Engels: Body cavity effusions
is one of the most aggressive types of lymphoma, but
can be treated in curative intention in most cases w6, 7,
19, 23, 30x.
Low grade lymphoma may cause serious diagnostic
problems, as it is often impossible to distinguish with cer-
tainty between a benign reactive effusion which shows a
predominance of stimulated lymphatic cells and a malig-
nant lymphoma only on the basis of cytomorphologic
methods. Therefore, in these cases additional immuno-
logic methods are indispensable using either immuno-
cytochemistry or flow cytometry of effusion fluid. This
problem occurs most often in serosal involvement by
chronic lymphocytic leukemia, lymphoplasmacytic lym-
phoma and marginal zone lymphoma.
In most cases, it is a comparatively easy task to dis-
tinguish follicular lymphoma from a benign effusion with
predominance of lymphocytes. Lymphoma cells of follic-
ular lymphoma show a typical morphology, which can be
observed in preparations of effusion fluid as well as in
samples of other origin. Nuclei are irregularly contoured
with one or more cleaves, the chromatin is paler and
more granular than that of normal lymphocytes, but not
blastic, as it is in cells of high grade lymphoma. Because
in every effusion some normal lymphocytes are found,
these may serve as an internal control and one may com-
pare the suspicious lymphatic cells with these normal
lymphocytes (Figure 4).
Cells of mantle cell lymphoma may be similar to cells
of follicular lymphoma. These two subtypes of lymphoma
usually cannot be distinguished only by cytomorphology.
Further immunologic studies are indispensable in these
cases w31, 32x.
In every case of suspected lymphoma, it is advisable
to review slides of peripheral blood and bone marrow, if
marrow involvement or leukemic course is known, and
Figure 4 Follicular lymphoma, normal lymphocyte at center, 100=, MGG (left). Malignant mesothelioma, 40=, MGG (right).
to compare the suspicious cells in effusion to cells of
diagnosed lymphoma in a patient.
Malignant mesothelioma produces malignant effusion
in nearly each case. Most common is involvement of
pleura (85% of all mesotheliomas), mesothelioma of peri-
toneum is occurring in a significantly smaller number of
cases (only 15%). Malignant mesothelioma of pericardi-
um is reported only rarely w33, 34x. In effusions a high,
and often extremely high, cellularity is observed. The
malignant cells resemble normal mesothelium more or
less strongly. Most times, enlarged nuclei, prominent
nucleoli and alterations of the cytoplasm are found. Fre-
quently small, clear vacuoles occur which may be con-
fluent and are located near to the nucleus like a ‘‘cap’’.
The atypical mesothelial cells occur in large, sometimes
extremely large, sheets or cohesive clusters. Rarely,
mesothelioma with preponderance of isolated tumor cells
is observed. In the background of smears, in some ca-
ses, a fine, granular material may be detected, which
stains pink in MGG stain. This representation is caused
by a high content of hyaluronic acid and looks exactly
like background staining in smears of synovial fluid which
always contains high levels of hyaluronic acid. These
findings are detected only in a small minority of cases,
but they are almost diagnostic of mesothelioma w6, 7, 19x
(Figure 4).
Every malignant process may involve serosal mem-
branes and produce an effusion. In addition to the neo-
plasms described above, malignant effusion may occur
in rare cases of a melanoma, different types of sarcoma
and germ cell tumors w35–40x.
Differential diagnosis
The following questions may cause serious difficulties in
differential diagnosis:
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1. In an effusion clusters of epithelial cells are detected
which display disturbed polarity of cells and perhaps
enlarged nucleoli – are they derived from benign
proliferating mesothelium, or carcinoma or
mesothelioma?
2. In an effusion large numbers of lymphatic cells are
present which appear to be mature – are they derived
from a benign effusion with lymphatic preponderance,
or from malignant lymphoma?
With regard to question 1, distinguishing between a
benign proliferation of mesothelium (which may occur in
the presence of inflammation or infarction) and carcino-
ma is not difficult. In a carcinomatous effusion two pop-
ulations of epithelium which are clearly separated from
each other are detected, normal mesothelium and a sec-
ond type of cells shed in sheets or clusters. Benign meso-
thelial cells may be present which show a remarkable
morphologic variability with continuous transition
between different functional stages of mesothelium.
Enlarged, sometimes even prominent nucleoli are
observed not infrequently in reactive conditions. Cells of
carcinoma do not blend into this morphologic continuum
of benign mesothelial cells and are easily recognized as
alien in most cases. There is no continuous transition
from mesothelial cells to cells of a carcinoma.
Differentiation between benign proliferating mesotheli-
um and malignant mesothelioma is easily done, if the
malignant cells display pronounced dysplastic features.
In some cases, discrimination between these two entities
is impossible solely by means of cytomorphology. A
strong indication towards malignant mesothelioma is an
extremely high cellularity of effusion in combination with
an occurrence of unusually large clusters. Clusters of
mesothelial cells containing more than 200 cells are sus-
picious for mesothelioma. Instead of two dissimilar pop-
ulations of cells, as observed in most carcinomatous
effusions, in mesothelioma only one population of epi-
thelium is detected with a continuous series between
normal-looking mesothelial cells and highly dysplastic
malignant cells.
With regard to question 2, in many cases this problem
cannot be solved only by means of cytomorphology. Fol-
licular lymphoma and mantle cell lymphoma show a typ-
ical morphology of their nuclei and usually are easily
recognized. Serosal involvement by lymphocytic lympho-
ma, lymphoplasmacytic lymphoma, or marginal zone
lymphoma cannot be distinguished from benign effusion
with predominance of lymphatic cells only by cytomor-
phology. Hence, in these cases an immunologic exami-
nation of effusion fluid is indispensable: either by
immunocytochemistry or by flow cytometry w31, 41x.
Conclusion and future prospects
Microscopic examination of pleural effusion, ascites, or
pericardial effusion is of great diagnostic value even
when limited to one or two routine stains. By means of
immunocytochemistry special questions may be
answered. As with all morphologic methods regular prac-
Engels: Body cavity effusions 423
tice and some experience are essential preconditions in
order to acquire a reasonable level of diagnostic certain-
ty. However, any such investment of time and labor into
cytomorphology is of value.
In clinical practice, empyema, perforation or fistula of
esophagus can be diagnosed quickly and reliably by
effusion cytology. Effusion of unknown origin in many
cases is the first manifestation of a malignant condition
not known before. Effusion cytology may provide indi-
cations to the primary tumor. In these cases, immuno-
cytochemistry offers the most valuable additional
method. In cases of already known malignant conditions,
effusion cytology may contribute important information
for staging and evaluating operability, e.g., in lung cancer.
By means of effusion cytology it is possible to select fast
and efficiently those patients in whom a thoracoscopy is
indicated among the large number of patients with pleu-
ral effusion.
Expression analysis of malignant cells and tissue by
microarray will presumably lead to important new infor-
mation about specific genetic aberrations during the
coming years not only concerning leukemia and lympho-
ma but also solid tumors. A significant increase of diag-
nostic tools for recognizing and classifying solid tumors
by FISH or by modified methods, such as silver in situ
hybridization or chromogenic in situ hybridization, can be
expected. Smears prepared from effusion fluid for cyto-
morphologic examination are well suited for these new
techniques.
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