Full text of DOI:10.1097/00005537-200211000-00014

The Laryngoscope
Lippincott Williams & Wilkins, Inc., Philadelphia
©
2002 The American Laryngological,
Rhinological and Otological Society, Inc.
The Clinical Value of Image Cytometry
DNA Analysis in Distinguishing Branchial
Cleft Cysts From Cystic Metastases of Head
and Neck Cancer
Sushma Nordemar, MD; Anders H o¨ gmo, MD, PhD; Johan Lindholm, MD, PhD; Edneia Tani, MD, PhD;
Bj o¨ rn Sj o¨ str o¨ m, MD, PhD; Gert Auer, MD, PhD; Eva Munck-Wikland, MD, PhD
Objectives/Hypothesis: A branchial cleft cyst pre-
sents as a lump in the neck that, generally, is easily
cured by surgical excision. The preoperative diagno-
sis is based on clinical examination and, especially in
the Scandinavian countries, fine-needle aspiration
cytology. However, at times, the histopathological
analysis of the excised cyst reveals a cystic metastasis
of squamous cell carcinoma of the head and neck. If
adequate diagnosis could be obtained preoperatively,
patients would most likely fare better. The study was
performed to investigate whether the diagnostic ac-
curacy for these lesions could be improved preopera-
tively by image cytometry DNA analysis of the fine-
needle aspiration cytology specimen. Study Design:
Image cytometry DNA analysis was performed on the
preoperative fine-needle aspiration cytology speci-
men and the surgical specimens from 51 patients with
solitary cysts in the lateral region of the neck. Thirty-
six patients were selected because there was a dis-
crepancy between findings on fine-needle aspiration
cytology and the final histopathological diagnosis or
an uncertain cytological diagnosis. There were 25
metastatic squamous cell carcinomas and 3 thyroid
cancers, there was 1 lymphoma and 1 sialoadenitis,
and there were 21 branchial cleft cysts. Methods: The
cytodiagnostic Giemsa-stained slides were destained
in Methanol and then stained with Schiff’s reagent.
The paraffin-embedded material from excised cysts
were cut and deparaffinized and then stained with
Schiff’s reagent. Ahrens image analysis was used for
DNA analysis and lymphocytes were used as control
cells. DNA valves exceeding 5c was regarded as ane-
uploid. Results: Image cytometry DNA analysis of the
preoperative cytological specimen was possible in 41
of 51 patients. We found that in 53% of the cases with
cystic metastasis, image cytometry DNA analysis,
when possible, revealed aneuploidy, thus indicating
malignancy. DNA analysis showed diploidy in all be-
nign cases. Conclusions: Aneuploidy is highly specific
for malignancy. Image cytometry DNA analysis in-
creases the diagnostic sensitivity for malignant cystic
metastasis and therefore is a valuable supplement to
conventional cytological study for these lesions. Key
Words: Image cytometry DNA analysis, branchial
cleft cysts, head and neck neoplasm, cystic
metastasis.
Laryngoscope, 112:1983–1987, 2002
INTRODUCTION
The most common cystic lesion occurring in the neck
is the branchial cleft cyst (BCC). Branchial cleft cysts
occur most frequently in the third decade of life and are
more frequent in male patients, and more than 75% of
cases present in the anterior triangle of the neck as a
persistent cystic swelling. Squamous cell carcinoma of the
head and neck (HNSCC) produces regional metastasis in
the deep cervical nodes. In the majority of cases, these
cases present as firm, solid masses in one of the desig-
1,2
nated lymph node levels. However, the metastatic car-
cinoma may undergo cystic degeneration and present as a
cervical cyst that mimics a BCC, especially when they
occur at levels II to IV and the primary cancer lesion is not
3–5
evident.
The differential diagnosis depends on the age of the
patient, and especially in patients over the age of 40 years,
the possibility of a metastatic cervical lymph node should
6,7
From the Departments of Otorhinolaryngology (S.N., A.H., E.M-W.) and
Pathology (J.L., E.T.) and the Cancer Centre (G.A.), Karolinska Hospital,
Stockholm, Sweden; and the Department of Otorhinolaryngology (B.S.),
Umeå Hospital, Umeå, Sweden.
be considered. There is also the possibility of a primary
cervical neoplastic cyst or “branchiogenic carcinoma,” al-
8,9
though this is rare. Detecting malignancy within a cyst
can be difficult. Radiological examination is generally not
helpful, and fine-needle aspiration cytology (FNAC) is not
Editor’s Note: This Manuscript was accepted for publication May 31,
2002.
Send Correspondence to Sushma Nordemar, MD, Department of
Otorhinolaryngology, Karolinska Hospital, S-17176 Stockholm, Sweden.
E-mail: sushma.nordemar@ks.se
10
always reliable. The false-negative rate of FNAC in cys-
tic lesions (i.e., when malignancy remains undetected) has
Laryngoscope 112: November 2002
Nordemar et al.: Branchial Cleft Cysts
1983

6
,11,12
been reported to range from 50% to 67%.
The mis-
men, the lesion was considered aneuploid if any aneuploid cell
nucleus was found.
taken diagnosis of a cystic metastasis has serious conse-
quences: The patient may not be urgently treated, the
search for a possible primary tumor is delayed, and the
surgical technique for a BCC differs considerably from
what is adequate surgical treatment when dealing with
neck metastasis.
Aberrant DNA values are seen in the majority of
cases of HNSCC when image cytometry (ICM) technique
is used in instances when single cell nuclei are investigat-
ed. The present investigation was undertaken to clarify
whether ICM DNA analysis contributes any diagnostic
information to conventional cytomorphological study of
FNAC specimens when a distinction between BCC and
cystic metastasis of HNSCC is required.
RESULTS
Image cytometry DNA assessments of the FNAC
specimen was possible in 41 of 51 cases. In the remaining
specimens, hypocellularity, cellular debris, inflammatory
cells, or initial handling and fixation made Feulgen stain-
ing and DNA analysis impossible.
Thirty-five patients had an initial diagnosis of BCC
after FNAC, but histopathological examination of the ex-
cised cyst revealed squamous cell carcinoma (SCC) in 18 of
them. Twelve of these 18 FNAC specimens could be DNA
analyzed, and 6 of them showed aneuploidy.
Eight patients had an inconclusive diagnosis after
FNAC (i.e., BCC or SCC). The histopathological examina-
tion of the excised cysts revealed SCC in six cases; one was
a BCC and one was a lymphoma. Image cytometry DNA
analysis of the FNAC specimens could be performed in
five cases. In three of the five cases of SCC, ICM DNA
analysis showed aneuploidy (60%), and the BCC specimen
on FNAC was diploid.
Six patients were diagnosed with SCC after FNAC,
but in five of them, histopathological examination of the
excised cysts revealed BCC. Image cytometry DNA anal-
ysis was diploid in all of these cases.
Image cytometry DNA analysis was possible in all
the excised cysts. Eighteen of 25 (72%) of the cystic me-
tastases showed aneuploidy. All 15 patients (mean age,
39 y [age range, 18–58 y]) in whom finding on both FNAC
and histopathological examination were benign were dip-
loid at DNA analysis (100%). The mean age of patients
with malignant cysts was higher (54.9 y) than for patients
with benign cysts (39.0 y) (Table I).
13
MATERIAL AND METHODS
Fifty-one patients (24 female and 27 male patients with a
mean age of 50.2 y) with a solitary cervical cystic lesion in the
lateral region of the neck who were referred to the departments of
otorhinolaryngology of the Karolinska Hospital (Stockholm, Swe-
den) and Umeå Hospital (Umeå , Sweden) from 1988 to 2000 were
included in the study. None of these patients presented any
clinically apparent head and neck cancer at the time of admis-
sion. Thirty-six of these patients were selected because of a dis-
crepancy between results of FNAC and the histopathological find-
ings of the excised cysts or uncertain cytological analysis, and 15
patients in whom both FNAC and histopathological examination
showed BCC were also investigated. Image cytometry DNA anal-
ysis was performed on the FNAC specimen obtained before sur-
gery, as well as on the surgically excised specimen from all
patients.
DNA Analysis
The cytodiagnostic slides (FNAC) stained with Giemsa were
destained in concentrated methanol. The slides were stored in
buffered 4% formalin overnight. The slides were rinsed in dis-
tilled water and subjected to acid hydrolysis (5N HCl, 22°C for
CASE REPORTS
1
h). After being rinsed in distilled water, they were stained with
Case 1
Schiff’s reagent at room temperature for 2 hours. They were
A 26-year-old woman (patient 5) presented with a few-
weeks’ history of a cervical swelling on the left anterolateral
region of the neck in December 1988. A complete otorhinolaryn-
gological examination did not reveal any malignancy. The 7 ϫ
5-cm mass was not tender, was movable, and was lying in the
anterosuperior triangle. Results of FNAC showed normal squa-
mous cells, macrophages, and inflammatory cells. The cytological
diagnosis was BCC. The cyst was excised in February 1989. The
histopathological diagnosis was metastatic SCC. Subsequent
panendoscopy and random biopsies could not localize any pri-
mary tumor site. The patient was given radiation therapy. In
December 1995, an SCC lesion at the left side of the tongue base
was noticed. The patient underwent a tongue base–pharyngeal
resection and had reconstruction with a free radial flap. DNA
analysis of the preoperative FNAC specimen in December 1988
and the excised cyst in February 1989 showed aneuploidy.
washed in distilled water and thereafter washed three times for
1
0 minutes in sodium bisulfite (10 mL 10% Na S O , 10 mL 1
2 2 5
mol/L HCl, 180 mL distilled water) and washed in tap water and
then in distilled water, and dehydrated in ethanol series and
14
xylene. The archival formalin-fixed, paraffin-embedded mate-
rial from the excised cysts was cut (4 ␮m), deparaffinized in
xylene, immersed in a descending ethanol series, and then stored
in buffered 4% formalin overnight. Thereafter, the slides were
treated as previously mentioned.
Evaluation of Nuclear DNA Content
For the quantitative DNA analysis, a densitometric device,
the Ahrens image analysis system (Bargtheide, Hamburg, Ger-
many), was used. This is a TV-based system equipped with a
charge-coupled device (CCD) video camera connected to a Nikon
microscope. In the excised specimen the DNA content of 100 cell
nuclei per specimen was registered. Lymphocytes were used as
Case 2
15
control cells to establish the normal diploid 2c value. Normal
diploid epithelial cells contain 2c DNA. Before mitosis the cell
increases its DNA content to 4c, but a nuclear DNA content
exceeding 5c is not normally seen in non-tumorous cell and is
therefore regarded as aneuploid. A surgically resected cyst in
which DNA analysis revealed greater than 5% aneuploid cell
nuclei was regarded as aneuploid, whereas in the FNAC speci-
A 79-year-old woman (patient 30) noticed a cervical swelling
on the right side in April 1999. She was referred to an otorhinolar-
yngologist in May 1999 after findings on FNAC showed SCC. Clin-
ical examination did not reveal any primary tumor within the head
and neck region. Computed tomography (CT) scan of the neck did
not show any disease other than the solitary cystic tumor in the
right anterolateral region of the neck. A new finding on FNAC in
Laryngoscope 112: November 2002
Nordemar et al.: Branchial Cleft Cysts
1
984

TABLE I.
Clinical, Cytologic, Histologic, and DNA-analysis Data of All Patients.
Patient
No.
Histology of
Excised Cyst
DNA-content
of FNAC
DNA-content of
Excised Cyst
Sex
Age (y)
FNAC
Primary Tumor
1
2
3
4
5
6
7
8
9
M
M
F
66
72
43
58
26
65
49
52
37
52
57
52
35
24
52
53
47
70
57
58
66
65
44
64
40
63
72
47
61
79
59
64
61
68
70
39
BCC
SCC
Aneuploid
Aneuploid
Aneuploid
Aneuploid
Aneuploid
Aneuploid
Diploid
Aneuploid
Diploid
Tonsil
BCC
SCC
Unknown
Tonsil
BCC
SCC
Aneuploid
Aneuploid
Aneuploid
Aneuploid
Diploid
M
F
BCC
SCC
Tonsil
BCC
SCC
Tongue base
Tongue base
Unknown
Tonsil
M
M
F
BCC
SCC
BCC
SCC
BCC
SCC
Diploid
Aneuploid
Aneuploid
Diploid
M
M
F
BCC
SCC
Diploid
Tonsil
1
1
1
1
1
1
1
1
1
1
2
2
2
2
2
2
2
2
2
2
3
3
3
3
3
3
3
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
BCC
SCC
Diploid
Unknown
Unknown
Unknown
BCC
SCC
Diploid
Aneuploid
Diploid
M
F
BCC
SCC
Diploid
BCC
Thyroid cancer
Thyroid cancer
SCC
Diploid
Diploid
F
BCC
Diploid
Diploid
M
M
M
M
F
BCC
Not possible
Not possible
Not possible
Not possible
Not possible
Not possible
Aneuploid
Aneuploid
Aneuploid
Diploid
Aneuploid
Aneuploid
Aneuploid
Aneuploid
Aneuploid
Aneuploid
Aneuploid
Aneuploid
Aneuploid
Diploid
Tonsil
BCC
SCC
Unknown
Nasopharynx
Tonsil
BCC
SCC
BCC
SCC
BCC
SCC
Palate
M
F
BCC
SCC
Tonsil
BCC/SCC
BCC/SCC
BCC/SCC
BCC/SCC
BCC/SCC
BCC/SCC
BCC/SCC
BCC/SCC
SCC
SCC
Tongue base
Unknown
Tonsil
F
SCC
M
M
F
SCC
SCC
Tonsil
BCC
Diploid
Diploid
M
M
M
F
SCC
Diploid
Diploid
Unknown
SCC
Not possible
Not possible
Diploid
Diploid
Nasopharynx
Lymphoma
BCC
Diploid
Diploid
F
SCC
BCC
Diploid
Diploid
M
F
SCC
BCC
Diploid
Diploid
SCC
BCC
Not possible
Diploid
Diploid
F
SCC
BCC
Diploid
F
SCC
Sialoadenitis
SCC
Diploid
Diploid
M
F
Sialoadenitis
Thyroid cyst
Not possible
Diploid
Diploid
Tongue base
Thyroid cancer
Diploid
BCC ϭ branchial cleft cyst; SCC ϭ squamous cell carcinoma.
July 1999 persisted in metastatic SCC. Results on panendoscopy
and nasopharyngeal as well as tongue base and ipsilateral tonsil-
lectomy in August 1999 were negative. The patient underwent a
neck dissection of the right side in September 1999. The histopatho-
logical diagnosis was BCC. DNA analysis of the preoperative FNAC
specimen as well as the BCC showed diploidy.
between benign and malignant cysts, and the absence of a
clinically detectable primary tumor makes the diagnosis
difficult.
Fine-needle aspiration cytology is a useful technique
when applied to solid cervical nodes because the false-
1
,18
positive and false-negative rate is low (1%–3%).
How-
ever, in cystic lesions it may be impossible to distinguish
the cytological features of a BCC from a cystic metastasis
of SCC. The aspirate from a cystic lesion can be difficult
DISCUSSION
Metastases from certain primary tumors of the oro-
pharynx, particularly SCC of the tonsil, are often cys-
3
6,16
tic.
The tendency for this tumor site to produce solitary
to interpret as a result of hypocellularity, large quantities
19
cystic metastasis while the primary tumor is still occult is
well documented and has led to misdiagnosis clinically
and cytologically.
of inflammatory cells, and cellular debris. Granstr o¨ m
6
and Edstr o¨ m in 1989 showed that cytological assessment
8,17
Palpation alone cannot distinguish
of the aspirate from cystic metastasis had a high false-
Laryngoscope 112: November 2002
Nordemar et al.: Branchial Cleft Cysts
1985

negative rate. They recommended ipsilateral tonsillec-
tomy in patients older than 40 years of age with a cervical
cyst because in their study, 80% of cystic metastases orig-
logical specimen. Because of the risk for overlapping of cell
nuclei, a 5c exceeding rate greater than 5% is requested
for aneuploidy. The cytological material from the fine-
needle aspirations in general contains a sparse amount of
cell nuclei for analysis, and the risk for undetected overlap
of nuclei is low, which is why the lesion was classified as
aneuploid if any aneuploid cell nuclei could be detected in
the FNAC specimen.
6,20
inated from an occult tonsillar carcinoma.
A false-
negative finding on FNAC leads to delay in searching for
the primary tumor site, as well as delay in the onset of
adequate oncological treatment. The surgeon violates the
neck while performing cyst excision and misses the chance
to take biopsy specimens from the most likely primary
tumor sites (i.e., tonsil, base of the tongue, and nasophar-
ynx) while the patient is under general anesthesia. Some
studies have shown that violating a neck by performing an
open biopsy of the cyst could not only delay the definitive
In the present study, 10 of 25 patients (40%) with
malignant histological findings (i.e., SCC) had the tonsil
as the primary site of the tumor. Although this is a lower
6
proportion than that found by Granst o¨ m and Edstr o¨ m,
this confirms the theory that malignancies in the tonsils
give cystic metastases to the neck in a higher rate than
other malignancies in the head and neck region.
21
treatment but also jeopardize cure. However, this fact
22
has also been questioned. On the other hand, when the
finding on FNAC is false-positive for malignancy, the
overtreatment that will be performed may cause unneces-
sary morbidity.
We do not know the incidence of SCC metastasis to
the neck masquerading as a BCC. In the Stockholm/Got-
land area of Sweden, a population of two million inhabit-
ants, approximately 40 patients with BCC are surgically
treated annually. Cystic metastasis from head and neck
cancer was found in 1 patient in the year 2000 and in 4
patients in the year 2001. There is reason to believe that
the risk increases with age and known risk factors for
head and neck cancer (i.e., smoking and alcohol use).
However, in our material we found both benign and ma-
lignant cystic lesions broadly overlapping age ranges; two
patients younger than 40 years of age had cystic metas-
tases, and five patients older than 59 years of age had
benign branchial cleft cysts. As a result of our findings, the
Stockholm Head and Neck Cancer Center has decided to
recommend ICM DNA analysis on the FNAC specimen
from all patients older than 30 years of age with a cystic
lesion in the lateral region of the neck. Furthermore, be-
fore surgical resection of the lesion, a panendoscopy is
performed to minimize the risk of missing a primary can-
cer lesion within the head and neck region.
Our study demonstrates the difficulties in assessing
a correct diagnosis of cystic neck lesions with only cyto-
logical examination, and that DNA analysis allows im-
proved diagnostic accuracy for these lesions. We had four
different groups of patients. In the first group of 20 pa-
tients, the finding on FNAC was benign (i.e., BCC) but
histopathological examination of the excised cysts re-
vealed malignancy. Eighteen cases were SCC; DNA anal-
ysis was possible in 12 cases and 6 of the 12 (50%) showed
aneuploidy. In the second group of eight patients, the
finding on FNAC was inconclusive BCC or SCC. Later
histopathological examination revealed SCC in six cases,
and DNA analysis showed aneuploidy in three of the five
lesions (60%) in which DNA analysis was possible. In the
third group of six patients, FNAC did indicate malignancy
but the results of histopathological examination were be-
nign. DNA analysis showed diploidy in all five lesions in
which analysis was possible (100%). Thus, if thyroid can-
cer cases are excluded, two-thirds (65%) of the patients in
whom it was possible to analyze the FNAC specimen
would have had benefit from an ICM DNA analysis pre-
operatively. Furthermore, all patients with BCC both on
FNAC and on histopathological examination displayed
only diploid cells.
CONCLUSION
Image cytometry DNA analysis appears to add valu-
able information to conventional cytological examination
in the diagnostic assessment of cystic lesions in the neck.
In our study, we found that 53% of SCC metastases
showed aneuploidy on FNAC indicating malignancy. The
risk for malignancy increases with age and risk factors,
and we recommend that ICM-DNA analysis should be
considered on all FNAC specimens from patients older
than 30 years of age as a supplementary tool in the clin-
icopathological assessment of these lesions so that appro-
priate therapy can be instituted primarily. Further, pan-
endoscopy preoperatively and, in suspect cases, frozen-
section analysis preoperatively should be used. Because
approximately 30% of SCC of the head and neck and many
thyroid cancer lesions are diploid, the ICM DNA analysis
will not be able to detect all malignant cystic lesions, and
a diploid result does not rule out malignancy. However,
our clinical experience clearly shows that the method is of
considerable use because when aneuploidy is found, ma-
lignancy should be expected and the patient treated
accordingly.
Image cytometry DNA analysis was performed on all
the FNAC specimens, but interpretation was possible in
4
1 of 51 patients, because of the sparse amount of cells
obtained by aspiration, necrosis, and technical difficulties
resulting from inadequate fixations, need for destaining,
and so forth. Our study is a retrospective study that was
performed on archived cytological material, and we sug-
gest that the cytologist should aspirate enough material
for at least three or four slides so that both conventional
cytological analysis and Feulgen staining for DNA analy-
sis can be performed primarily. The initial handling with
immediate rinsing from the specimens of blood, mucus,
and external contaminants and adequate fixation is im-
portant. DNA analysis is easier to perform on freshly
obtained FNAC specimens than on archival material be-
cause the destaining procedure itself is difficult and time-
consuming and may hamper the Feulgen staining.
When DNA analysis is performed on a resected cyst,
it is in fact the cyst wall that is examined as a histopatho-
Laryngoscope 112: November 2002
Nordemar et al.: Branchial Cleft Cysts
1
986

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