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Fine-Needle Aspiration Cytology in the Diagnosis of Tuberculous Lesions

Article  in  Laboratory Medicine · November 2000

DOI: 10.1309/UJ0B-VDWV-U0LE-E0QQ

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CYTOLOGY
Dilip K. Das, MD, PhD, FRCPath

Fine-Needle Aspiration
Cytology in the Diagnosis of
Tuberculous Lesions
Globally, mycobacterial disease, including tuber- ABSTRACT Fine-needle aspiration (FNA) cytology is a
culosis (TB) and nontuberculous mycobacterial simple, economical, highly accurate tool in the diagnosis of

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infection, is now the leading infectious cause of tuberculous lesions. It is also ideal for sample collection for
morbidity and mortality. In contrast to invasive
ancillary studies such as Ziehl-Neelsen (Z-N) stain for acid-
procedures like core-needle biopsy, excision
biopsy, and laparoscopic biopsy, which have been fast bacilli (AFB), as well as culture, radiometric, and
advocated for collection of specimens in extrapul- molecular biologic studies of Mycobacterium tuberculosis.
monary tuberculosis for histopathologic and The cytologic diagnosis of tuberculous lesions depends upon
mycobacterial studies, fine-needle aspiration demonstration of epithelioid granuloma with or without
(FNA) cytology is a simple and economic tool necrotic material in the smear. In studies involving multiple
with high diagnostic accuracy for tuberculous
sites, AFB positivity by Z-N or fluorochrome stain ranges
lesions. It has been used for the diagnosis of tuber-
culous lesions presenting as superficial lumps and from 23% to 45% with an average of 35.5%. The positive
bumps, ulcers, and sinuses, and for deep-seated, rate of mycobacterium culture from FNA material ranges
space-occupying lesions under imaging guidance. from 20.8% to 83% with an average of 57.6%. A few

Scientific Communications
As in histology, FNA cytodiagnosis of mycobacte- limitations include sampling and interpretation error and
rial diseases depends on demonstration of epithe- differential diagnostic problems.
lioid granuloma and/or necrotic material.
over a 34-year period—5% annual decrease in
Magnitude of the Problem new cases of TB—was reversed in 1985.4 Between From the
Department of
As an epidemic, TB has superseded its medieval 1985 and 1991, the number of cases increased 18% Pathology, Faculty of
cousins, plague and cholera, and whole conti- nationwide, and the increase was noted mainly Medicine, Kuwait
nents, much like Europe in the 19th century, are within groups and in geographic areas where HIV University, Kuwait.
again threatened by this scourge.1 The World infection is prevalent, suggesting that a large pro- Address
Health Organization estimated in 1990 that one portion of these “excess cases” are occurring in correspondence to

4
third of the world’s population, or 1.7 billion peo- HIV-infected individuals.5 Groups at high risk of Dr Das, Department

Section
of Pathology, Faculty
ple, were infected with the causative organism TB include not only HIV/AIDS patients, but also
of Medicine, Kuwait
Mycobacterium tuberculosis, and from this pool, 8 the very young (infant through age 4), infirm University, PO Box
to 10 million new active cases emerge annually, the elderly people, and other immunocompromised 24923, Safat, 13110
majority of which are communicable forms of subjects, such as organ transplant recipients and Kuwait.
pulmonary disease.2 cancer patients receiving chemotherapy. Recogni-
In 1993, approximately 3 million people died of tion of these high-risk groups is vital for diagno-
TB, and over the next decade there will be about sis, prevention, and control programs.2
90 million new cases and 30 million deaths unless
the response to the global TB problem improves
radically.3 The problem is not limited to develop-
ing nations alone, where half the population is
infected; the trend established in the United States

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 Diagnosis made it possible to sample even deep-seated extra-
The lung is the most common site affected by TB pulmonary TB lesions in liver and spleen,28 intes-
in humans, but isolated extrapulmonary organ tine,29 pancreas,30 adrenal glands,31 prostate,32
involvement is well known; common sites include and bone, including spine,33,34 by FNA. A few
lymph nodes, kidney, long bones, genital tract, studies are based on multiple body sites.9,35-38 FNA
brain, and meninges.6 Lymphadenitis, characteris- averts the physical and psychological trauma occa-
tically involving the cervical chain (scrofula), par- sionally encountered with open surgical biopsy: it
ticularly the right anterior nodes, is the most is convenient for patient and physician alike, it can
common form of extrapulmonary tuberculosis, be performed on outpatients, it is relatively pain-
and about a third of these patients have TB at less, and it provides good correlation between
other sites.4 cytomorphologic and histopathologic features.18
A careful history and physical examination Endoscopic FNA cytology has been used for the
often suggest the diagnosis of pulmonary TB.7 diagnosis of pulmonary39 and gastrointestinal
Although sputum smears for acid-fast bacilli tract lesions.40 A luminal lesion may frequently be
(AFB) and cultures are the most specific compo- associated with inflammation and necrosis in its

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nents of diagnosis, the former is not very sensitive, superficial aspect. Whereas a needle biopsy for
as the likelihood of a positive smear depends heav- histopathologic examination may not yield a rep-
ily on the extent of pulmonary involvement.2 resentative specimen in such a situation, FNA can
Thus, culture examination is desirable for estab- collect cells from the deeper areas and even
lishing the diagnosis before instituting treatment.8 beyond the wall of the viscera to facilitate a proper
Culture, positive in 95% of patients,4 is considered tissue diagnosis. At times, cases of TB present as an
the diagnostic gold standard. However, current ulcer or a draining sinus. FNA cytology is a useful
methods typically entail 3 to 6 weeks to cultivate tool for sample collection and obtaining a diagno-
and identify species; more rapid cultivation and sis in these cases.41
identification techniques that use radiometric, Gross and microscopic features of tuberculous
molecular biologic, or chromatographic methods2 lesions in fine-needle aspirates are well docu-
are not readily available. mented in literature. Metre and Jayaram15
Extrapulmonary TB, a much more obscure described the gross appearance of the aspirates as
process, is more difficult to diagnose than pul- blood-mixed, cheesy, and purulent. As with histo-
monary TB. The tissue diagnosis, including bacte- logic sections of granulomas, which consist of a
riologic confirmation of the tuberculous nature of necrotic center surrounded by epithelioid histio-
the process, usually requires invasive procedures cytes and giant cells,42 FNA cytologic diagnosis of
that are likely to be associated with complications, lesions likely to be of tuberculous etiology or due
and the number of organisms in extrapulmonary to nontuberculous mycobacteria (NTM) requires
lesions is generally small.5 For this reason, FNA demonstration of epithelioid granuloma with or
cytology can serve as a useful diagnostic tool. without necrotic material. Based on the morpho-
logic features, Bailey and associates35 distin-
Value of Fine-Needle Aspiration guished 2 groups: cases with distinct epithelioid
FNA cytology is a simple and economic procedure granuloma and those in which no granulomas
for diagnosis of TB compared with core-needle were found, but large amounts of necrotic debris
biopsy or excision biopsy, not only at the initial with variable numbers of polymorphonuclear
stage, but also during follow-up of patients after cells, histiocytes, and lymphocytes were observed.
treatment with an antitubercular regimen. FNA Qadri and associates36 catagorized the lesions
offers a wider scope for diagnosis of organ and tis- as caseating and noncaseating granulomas and
sue involvement.9 In the past 2 to 3 decades, a found an excellent cytohistologic correlation.
large number of reports on FNA cytologic diagno- Three major groups were described, by Das and
sis of pulmonary TB8,10-14 and tuberculous lesions colleagues,14,17,37,43 Das and Pant, and Radhika et
of extrapulmonary superficial sites, such as lymph al38 (Table 1). Type I is epithelioid granuloma
nodes,15-22 breast,23,24 thyroid,25,26 and salivary without necrosis (Fig 1A), type II is epithelioid
gland,27 have been published. Imaging aids have granuloma with necrosis (Fig 1B), and type III is
necrosis without epithelioid granuloma (Fig 1C).
At times, there is neutrophilic infiltration in

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 Table 1. Cytologic Features and Acid-Fast Bacilli (AFB) Positivity in
Fine-Needle Aspiration (FNA) of Tuberculous Lesions*
Site of FNA/ Cytologic Features AFB Positivity
(Investigators) No. of Cases (% of Cases) (% of Cases)(Z-N Stain)
Type I Type II Type III Type I Type II Type III Overall
Lung (Das et al14) 38 10.5 44.7 44.7 0.0 38.5 60.0 45.8
Lymph node (Das et al17) 174 25.3 39.1 35.6 9.1 64.7 77.4 55.2
Breast (Das et al43) 30 10.0 53.3 36.7 0.0 25.0 36.4 28.0
GI tract (Das and Pant29) 23 47.8 30.4 21.7 0.0 0.0 40.0 10.5
Abdomen (Radhika et al38) 105 47.6 34.3 18.1 30.0 55.5 63.1 44.8
All sites (Das et al37) 574 31.5 31.9 36.6 5.4 30.0 48.5 30.8
Averages 28.8 39.0 32.2 7.4 35.6 54.2 35.9
GI indicates gastrointestinal; Z-N, Ziehl-Neelsen.
*Type I indicates epithelioid granuloma without necrosis; type II, epithelioid granuloma with necrosis; type III, necrosis without
epithelioid granuloma.

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Scientific Communications
A B C
Fig 1. A, Epithelioid granuloma without necrosis: lymph node aspirate showing a group of epithelioid cells and 1 Langhans giant cell. Stain
for acid-fast bacilli (AFB) was negative (H&E, 3400). B, Epithelioid granuloma with necrosis in the aspirate from a lung lesion. Stain for
AFB was positive (May-Grünwald-Giemsa, 3400). C, Necrosis without epithelioid granuloma: necrotic material with moderate neutrophilic

4
reaction from a swelling in the thyroid region shown in Fig 2C. Stain for AFB was positive (May-Grünwald-Giemsa, 3200).

Section

necrotic material, which may be so intense that it The studies on FNA diagnosis also provide
suggests an acute suppurative lesion. Type II reac- information about the frequency of tuberculous
tion, epithelioid granuloma with necrosis, is the lesions at different sites (Table 2). In developing
most common type followed by type III and type I countries like India, where TB is rampant, tuber-
reactions. In addition to these 3 groups, a fourth culous lymphadenitis (Fig 2A) continues to be the
group comprising poorly developed/doubtful most common type of lymphadenitis (30.0%-
epithelioid cells or occasional epithelioid cells with- 51.6%) encountered in clinical practice18 and in
out characteristic necrosis/giant cells has been lymph node FNA specimens.36,37 Patients may
adopted by a few groups of investigators.18,20 present with healed sinuses and ulcers (Fig 2B).
Even the thyroid gland, once thought to be resis-
tant to TB, is found to contain tuberculous lesions

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 Table 2. Fine-Needle Aspiration (FNA) Cytology Diagnosis of
Tuberculosis Lesions and Their Frequency in Various Organs
No. of Cases No. of Cases
Site With FNA Cytology with Tuberculous Lesions (%) Investigators
Lung 190 38 (20.0) Das et al14
374 18 (4.8) Gomes et al13
Lymph nodes 1,471 560 (38.07) Gupta et al18
875 277 (31.6) Gupta et al20
Breast 1,061 30 (2.8) Das et al43
410* 14 (3.4) Nayar and Saxena23
Thyroid 1,283 8 (0.62) Das et al25
1,565 18 (1.15) Mondal and Patra26
GI tract 78 23 (29) Das and Pant29
Prostate 567 34 (6.0) Mondal et al32
Salivary gland 160 10 (6.2) Shaha et al27

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GI indicates gastrointestinal.
*Comprised breast lump FNA and nipple discharge smears.

A B C
Fig 2. A, Tuberculous lymphadenitis: multiple enlarged lymph nodes in right cervical lesion. Fine-needle aspiration yielded epithelioid cells
and necrotic material, but the stain for acid-fast bacilli was negative. B, Tuberculous ulcers in medial aspect of left thigh. Fine-needle
aspiration yielded epithelioid cells and giant cells. The stain for acid-fast bacilli was positive. C, Tuberculous thyroiditis with swelling in the
thyroid region. Microscopic features are depicted in Fig 1C.

(Fig 2C) (0.6%-1.2% of all thyroid aspirates).25,26 Various ancillary techniques used for cytodiag-
Other notable extrapulmonary sites affected by nostic confirmation include demonstration of the
tuberculous lesions and diagnosed by FNA cytol- causative organism, M tuberculosis or NTM, by
ogy include gastrointestinal tract (Fig 3A) and Ziehl-Neelsen (Z-N) stains and fluorochrome
associated organs, breast (Fig 3B), and prostate technique, and by culture or molecular biology.
and salivary glands; even the pancreas may be FNA is a suitable tool for collection of material for
affected (Fig 3C). such investigations. In studies involving multiple
sites, AFB positivity by Z-N or fluorochrome stain
ranges from 23.0% to 45% with an average of
35.5%.9,35-38 AFB positivity for lymph node by Z-
N staining varies from 25% to 88.7%, with an

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A B C
Fig 3. A, Intestinal tuberculosis: fine needle aspiration from a bowel mass shows a group of epithelioid cells, intestinal epithelium, and
mucin (May-Grünwald-Giemsa, 3128). B, Tuberculous mastitis. Fine-needle aspiration from a breast mass shows epithelioid cells, scanty
necrotic material with dense inflammatory cell reaction, and a group of benign duct cells (May-Grünwald-Giemsa, 3200). C, Fine-needle
aspirate from a pancreatic mass showing epithelioid cells and a group of benign pancreatic acinar cells (May-Grünwald-Giemsa, 3200).

average of 52.9%.15,17,20-22,44 For breast, a wide choice for NTM adenopathy. The aspirate can also
variation is frequency is also seen, ranging from be used for radiometric assays and molecular biol-
12% to 100% with an average of 46.7%.24,43,45 The ogy techniques, including new rapid diagnostic
reported AFB positivity for other sites includes methods using labeled RNA or DNA probes,
lung, 45.8%14; gastrointestinal tract, 10.5%29; thy- which allow immediate species identification of
roid, 62.5%25; and bone and soft tissue, 64.0%.33 isolates of mycobacteria.4

Scientific Communications
The finding of AFB positivity in an increasing The approach to cytodiagnosis of TB in various
order in the 3 cytologic groups described by Das studies is basically similar. According to Gomes et
and others14,17,37,43 Das and Pant,29 and Radhika al,13 a sample is called diagnostic when Z-N stain
et al38 (epithelioid granuloma without necrosis and/or culture is positive, suggestive when there is
[average, 7.4%], epithelioid granuloma with granulomatous inflammation, and inconclusive
necrosis [average, 35.6%], and necrosis without when there is nonspecific inflammation or iso-
epithelioid granuloma [average, 54.2%]) corrobo- lated giant cell or blood elements. According to
rate the tissue response in pulmonary tuberculosis Das et al,17 when AFB is positive in a smear con-
as described in standard histopathology text- taining epithelioid granuloma and/or necrosis, it
books.42,46,47 is diagnostic of a tuberculous lesion. When AFB is

4
Culture examination is important for identi- negative in the presence of epithelioid granuloma
Section
fying atypical mycobacteria8 and for determina- in a developing country like India, it is considered
tion of drug sensitivity or resistance since the a granulomatous lesion likely to be of tuberculous
emergence of multidrug resistant TB due to inef- etiology, and culture for mycobacterium is
fective treatment and tubercle bacilli mutation advised. When the smear contains only necrotic
pose a great challenge.48 The positive rate of material with or without inflammatory cells and
mycobacterium culture from FNA material AFB is negative, it is advisable to exclude TB by
ranges from 20.8% to 83%, with an average of mycobacterium culture and even by a therapeutic
57.6%.20,33,35,36,38 Margileth and associates49 trial, if needed. In such a situation, the demon-
observed that chronic lymphadenopathy due to stration of mycobacterial antigen by immunocy-
mycobacterial infection is caused more frequently tochemistry may be of use.22
by NTM than by M tuberculosis, and the correct
diagnosis of TB vs NTM disease is essential, since
antituberculous therapy is effective for TB adeni-
tis, while excisional biopsy is the treatment of

N OV E M B E R 2 0 0 0 VO L U M E 3 1 , N U M B E R 11 L A B O R ATO RY M E D I C I N E 629
 Limitations of Fine-Needle Aspiration induce inflammatory reactions, including multin-
Although cytodiagnostic parameters of TB are ucleated giant cells, and create confusion with
well defined, the process is not without limita- granulomatous lesions.57,64 TB and malignant
tions. There is chance of technical as well as inter- neoplasm may also coexist,65,66 and if proper sam-
pretative error in the FNA cytologic diagnosis of pling is not done in these situations, one of these
TB. The sample may not be representative or ade- lesions may be missed.67
quate in the case of small pulmonary lesions or in
cases associated with fibrosis. FNA diagnosis of Conclusion
pulmonary TB is more suited to evaluation of Five decades of TB control programs using what
nodules or lesions in which there is suspicion of were considered to be efficacious drugs have failed
malignancy.50 In such a situation, the cytopathol- to reduce the incidence and prevalence of TB infec-
ogist usually concentrates on finding malignant tion and disease in most parts of the world. With the
cells in the smears and, as a result, may miss a emergence of a TB-friendly HIV, we may see many
small amount of necrotic material with or without more cases of TB, with greater risk of transmission
a few epithelioid cells.14 of the bacillus to others and a maintainance pool of

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In cases presenting as a cold abscess, well- infection at the level of a third of the world popula-
formed epithelioid granulomas may not be seen. tion.68 The effective implementation of available
Poorly formed granulomatous reaction may also treatment and preventive measures for TB on a
be seen in HIV-positive patients affected by global scale and research into new diagnostic and
Mycobacterium avium-intracellulare. Diagnosis of therapeutic tools and vaccines should be interna-
such lesions based solely on FNA cytomorpho- tional health priorities.69 Because diagnosis is an
logic features may be difficult. Differentiating important part of this process, and because FNA is a
tubercle bacilli from other mycobacteria such as M useful tool for routine cytodiagnosis with diagnostic
avium-intracellulare may be problematic unless accuracy ranging from 84.2% to 100%19,21,70,71 and
cultures are used.51 for collection of samples for ancillary studies, it is
Differential diagnostic problems may arise necessary to expand this use of FNA through estab-
because of the presence of cytologic components lishment a network of cytology laboratories.l
such as epithelioid cells, multinucleated giant
cells, and necrotic material individually or in com- Acknowledgment
bination in lesions other than those associated I thank James Luke for secretarial help in preparation of the
manuscript.
with TB (sarcoidosis,52 leprosy,53 mycosis,54 sili-
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