Int. J. Oral Maxillofac. Surg.

2006; 35: 324–331

doi:10.1016/j.ijom.2005.07.019, available online at http://www.sciencedirect.com

Clinical Paper
Head and Neck Oncology

Observation of tumour A. K. Songra, S. Y. Ng, P. Farthing,

I. L. Hutchison, P. F. Bradley
Maxillofacial Unit, Royal London Hospital,

thickness and resection margin Barts and The London NHS Trust, London E1
2BB, UK

at surgical excision of primary

oral squamous cell carcinoma—
assessment by ultrasound
A. K. Songra, S. Y. Ng, P. Farthing, I. L. Hutchison, P. F. Bradley: Observation of
tumour thickness and resection margin at surgical excision of primary oral squamous
cell carcinoma—assessment by ultrasound. Int. J. Oral Maxillofac. Surg. 2006; 35:
324–331. # 2005 International Association of Oral and Maxillofacial Surgeons.
Published by Elsevier Ltd. All rights reserved.

Abstract. Tumour thickness and the status of resection margins are of prognostic
significance in the treatment of oral cancer. In a single blind prospective study,
14 patients with biopsy proven oral squamous cell carcinoma had intraoral
ultrasound imaging done preoperatively to measure tumour thickness, and
intraoperatively to measure the deep surgical margin half way during resection. The
cut surface was demonstrated on ultrasound by placing a metal, ultrasound-
reflective, retractor into the surgical cut. The ultrasound measurements were
compared to the subsequent histological measurements. Using the threshold of
5 mm as indicator of margin clearance, there was agreement in 10 out of 14 cases
between ultrasound and histology. Ultrasound detection of close surgical margins
had a sensitivity of 83% and a specificity of 63%. For preoperative tumour thickness Key words: tumour thickness; margin clear-
ance; oral cancer; intraoral ultrasound imaging;
measurement, ultrasound imaging showed a high degree of correlation with
intraoperative ultrasonography; intraoperative
histology (Pearson correlation coefficient = 0.95, P < 0.01). This original paper guidance.
demonstrates that high resolution ultrasound imaging applied intraorally is a
reliable tool in objectively assessing both the tumour thickness and the surgical Accepted for publication 26 July 2005
margin clearance at the time of surgery. Available online 13 December 2005

Among the large number of prognostic
factors demonstrated to be of importance
in the treatment of oral squamous cell
carcinoma are tumour thickness and the
status of the resection margins. Achiev-
ing tumour clearance at the primary site
is a major problem but a very important
aspect of cancer surgery. It has been
shown by numerous studies that patients
demonstrating invasive carcinoma at
resection margins have a higher inci-
dence of loco-regional recurrence and
reduced survival rate12. Controversy
exists regarding the value of posto-
perative radiotherapy following incom-
plete excision12,22. Complete removal of
the primary tumour at the first attempt
will obviate the need for adjuvant

0901-5027/040324 + 08 $30.00/0 # 2005 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
 Resection margin by ultrasound 325

radiotherapy in most cases and maximise ments and a trend to use various ultrasound machine used was HDI 5000
prognosis. imaging modalities for the guidance of (Advanced Technologies Ltd., Seattle).
Visual inspection and palpation at the tumour surgery. However, there is no The ultrasound probe used was the broad-
time of surgery in addition to a number of study showing the value of intra-oral, band, linear 5–10 MHz Small Parts probe,
pre-operative modes of imaging all have intra-operative, ultrasound imaging in with a footprint of 26 mm. This was
their limitations in ensuring complete guiding resection of oral cancer. designed for intra-operative use and was
resection of a tumour mass. Frozen section The purpose of our original study is to small enough to be used intra-orally. It was
control although widely used has its pro- assess the depth of invasion or thickness of contra-angled which allowed good access
blems3,14,15. It cannot be used to study an oral cancers with the use of intra-oral ultra- to most parts of the oral cavity.
entire margin and cannot demonstrate the sonography and to observe the deep surgi- The intra-operative ultrasound scanning
amount of clearance. There are difficulties cal margin at the time of surgery, halfway was performed in order to:
in deciding where to take the sample and in during resection. This is an observational
localising the biopsy site to the specimen. study to see whether ultrasound can accu- 1. measure the tumour thickness,
Processing samples is very time-consum- rately predict if the surgical margin is 2. measure the deep margin clearance.
ing and may preclude its routine use. involved, close or clear of the tumour at
One of the current limitations of achiev- the time of resection, and then correlated A trained radiologist (SN) and a trained
ing margin clearance is the lack of an with subsequent histological analysis. As surgeon (AS) carried out all the scanning.
imaging technique to measure the thickness an observational study and to avoid subject Wherever possible, the ultrasound mea-
of the primary tumour. Clinical judgement bias (Hawthorn effect), the surgeons were surements were carried out using a non-
has been shown to be unreliable, as evi- asked to perform their resection as per contact technique, i.e., without the ultra-
denced by the number of resections that are normal and were not informed of the ultra- sound probe touching the tumour surface.
reported with involved margins10,12. Ima- sound results. This methodology has not Any gaps between the probe and the tumour
ging techniques such as CT and MRI do not previously been reported. surface were filled with normal saline, as
have the resolution to demonstrate the ultrasound waves do not travel through air.
thickness of primary oral cancer accu- Access to posteriorly located tumours on
rately17. Lack of pre-operative information Method the tongue was achieved by retraction aided
regarding tumour thickness leads not only by a suture. For tumours of the tongue
to possibly inadequate resection, but Ethical approval from East London and (n = 11), tumour thickness and deep margin
increases the risk of local recurrence and City Health Authority was obtained for the clearance measurements were always
reduces the survival rate12,18. use of ultrasound imaging intra-opera- made in the axial plane and also, where
High resolution diagnostic ultrasound tively in oral cancer patients. accessible, the coronal plane.
imaging is becoming well established in This was a single blind, prospective The deep margin assessment was carried
the field of head and neck oncology5,13,21. study performed between 1997 and 2002. out half way through surgical resection. In
There are many studies describing the ultra- Pre-operative tumour thickness measure- order to demonstrate the cut margin on
sound features of metastatic cervical lymph ments by ultrasound imaging were per- ultrasound, an echogenic surface, such as
nodes23, but not of the primary site. Trans- formed in 26 patients with biopsy proven a metal retractor, was placed in the surgical
cutaneous extra-oral (through skin and oral SCC and who were previously cut (Figs 1–3). Only light pressure was
muscles of submental region) ultrasound untreated. In 14 of these patients applied when holding the ultrasound probe
imaging of the tongue has been carried out (Table 1), we then carried out intra-opera- next to the tumour surface, so as to avoid
in some early studies2. However, such an tive ultrasound imaging during resection. compressing the tissues. In some cases,
extra-oral approach can only measure Case selection depended on the availability when a gap appeared between the cut mar-
approximate thickness and only when the of an ultrasound specialist (SN). The gin and the metal retractor; it would be
tumour is large. Transcutaneous ultrasono-
graphy is considered inferior to intra-oral
Table 1. Ultrasound and histological measurements of tumour thickness and of surgical margin
ultrasonography8. With improvements in clearance (n = 14)
imaging technology and availability of high
frequency, high resolution, intra-oral ultra- Tumour Surgical
thickness margin
sound probes, it is now possible to make
accurate measurement of the thickness of Patient code Tumour site TNM stage U/s Hist. U/s Hist.
primary oral cancer. SHINTANI et al.16 1 Tongue T1 N0 M0 15.0 14.0 4.0 7.0
showed that there is good correlation 2 Tongue T1 N0 M0 2.3 1.5 1.5 1.7
between intra-oral ultrasound thickness 3 Alveolar mucosa T1 N0 M0 2.0 1.4 1.0 0.9
measurement of tumours and histological 4 Tongue T2 N2a M0 8.0 11.8 1.9 3.2
thickness of tumours. SHINTANI et al.17 5 Lip T1 N0 M0 4.0 3.0 3.0 4.5
showed that ultrasound is superior to CT 6 Tongue T4 N3 M0 25.0 21.0 2.0 4.0
7 Tongue T1 N0 M0 4.4 2.2 3.2 8.0
and MRI for measurements of tumour 8 Tongue T2 N0 M0 10.0 11.0 6.6 7.5
thickness, especially those of less than 9 Tongue T2 N2a M0 8.0 9.6 15.6 13.0
5 mm20. HELBIG et al.7 carried out a small 10 Tongue T2 N0 M0 13.4 10.0 3.7 7.5
study in five patients using ultrasound for 11 Tongue T1 N0 M0 7.3 7.0 7.0 5.0
intraoperative visualization and marking of 12 Floor of mouth T1 N0 M0 0.5 4.0 6.0 5.0
tumour margins prior to resection. 13 Tongue T2 N1 M0 12.3 9.0 7.8 3.0
There is an increasing number of studies 14 Tongue T1 N0 M0 4.4 5.0 7.2 15.0
investigating the usefulness of ultrasono- Patient 1 is featured in Fig. 2a–c. Patient 9 is featured in Fig. 1a–c. All measurements are in
graphy for tumour thickness measure- millimetres.
326 Songra et al.

Fig. 1. (a) Partially resected tongue tumour (B) with metal instrument (C) in the cut to provide a surface to reflect ultrasound. Ultrasound probe (A)
is placed on the surface of tongue (labels match diagram in Fig. 3). Patient 9 in Table 1. (b) Ultrasound image of part (a). Note 2 pairs of electronic
cursors to measure the distance from tongue surface to the deep margin of the tumour, and from the latter to the surgical cut. Field width: 26 mm.
(c) Line diagram of part (b). S: tongue surface. T: tumour. M: metal instrument (bright white line). D: deep surgical margin. The surgical margin is
clearly shown to be separate from the hypoechoic tumour. The gap between D and M is filled with water during ultrasound imaging. Note 2 pairs of
cursors to show where measurements were made.

filled with water thus excluding air (Fig. 1b margin and the metal retractor (Fig. 3). The them. Patience and skill were always
and c). The probe was carefully angulated best images were acquired when the latter required. Once a good image was obtained,
to obtain an image which clearly showed three planes were parallel to each other and pairs of electronic cursors were placed on
the tumour deep margin, surgical resection the ultrasound beam was at 908 to all of the (pre-calibrated) ultrasound screen and
 Resection margin by ultrasound 327

Fig. 2. (a) Partially resected tongue tumour with ultrasound-reflective instrument in the cut. Patient 1 in Table 1. (b) Ultrasound image of part (a). In
this case, the surgical cut is quite close to the deep margin of the tumour, rendering the latter difficult to delineate (see Fig. 4 for macroscopic specimen).
Field width = 26 mm. (c) Line diagram of part (b). T: tumour. M: metal instrument. Note 2 pairs of cursors to show where measurements were made.

the following measurements made along a
line at 908 to the tumour surface:
1. from tumour surface to deepest point
on deep tumour margin;
2. from deepest point on deep tumour
margin to surgical margin.
As this was an observational study, the
ultrasound measurements were not com-
municated to the surgeon performing the
operation. In this single blind study, the
operating surgeon performed surgery as
per usual, without being told of the ultra-
sound measurements of marginal clear-
ance. The histopathologist was not given
prior knowledge of any of the ultrasound
measurements.
Following resection, the fresh specimen
was scanned by ultrasound to assess the
entire tumour and its relationship to all the
margins. The surface of the tumour was
marked with indelible ink opposite the site
of the greatest depth, at which ultrasound
measurements had been made. After the
specimen was fixed, it was re-scanned by
ultrasound. When possible, the specimen
was cut by the histopathologist in the pre-
sence of the surgeon or the radiologist in
order to guide the histologist to specific
areas of interest (Fig. 4). This did not con-
travene the single blind nature of this study
as only specimen orientation information
328 Songra et al.

mended by the Royal College of

Fig. 3. Diagram of partially resected tumour (B) being assessed by ultrasound for depth clearance,
with a reflective instrument (C) in the surgical cut. A: ultrasound probe (contra-angle).
was discussed, not tumour depth and clear-
ance information. After histological pre-
paration, the histopathologist measured
the tumour thickness and the surgical mar-
gin clearance at the point marked with
indelible ink without knowledge of the
ultrasound measurements. Routine histolo-
gical examination was then performed,
including checking for clearance at all mar-
gins using the histological criteria recom-
Pathologists for histological grading of
surgical margin.
For a tumour to be classified as com-
pletely excised, it must have a histological
tumour-free margin of greater than 5 mm.
A tumour-free margin of less than 5 mm is
considered to be close, and that less than
1 mm is considered to be involved.
The ultrasound findings were compared
to the histological findings and various
statistical analyses performed. Scatter plots
of data with regression lines were obtained.
Two correlation tests were performed on
the distance measurements data in order to
determine the overall correlation between
them. The Kappa test was done to calculate
the sensitivity, specificity and predictive
value of using ultrasound imaging to deter-
mine whether the surgical margin was close
or clear, where a close margin was defined
as less than 5 mm, and a clear margin was
greater or equal to 5 mm.

Fig. 4. (a–c) Macroscopic specimen (a) and diagram (b) of excised tongue squamous cell carcinoma (same case as in Fig. 2). In part (b), note
proximity of deep tumour margin T to the surgical margin Q. S: surface of tongue and of tumour. Part (c) is the ultrasound image of the tumour
before excision. Note how well the tumour outline matches that in the macroscopic specimen.

Fig. 5. Scatter plot of tumour thickness measurements by ultrasound and by histology. Note the
plotted points nearly all lie on a straight line, showing a strong positive relationship (P < 0.01).
Results Applying the threshold of 5 mm to indi-
cate whether the deep surgical margin was
Table 1 shows the measurements of tumour clear of tumour, there was agreement in 10
thickness and of deep margin clearance by out of 14 cases between ultrasound and
ultrasound scanning and by histology. histology (Table 2). Using ultrasound to
Figure 5 is a scatter plot of tumour thickness detect close surgical margins resulted in
measurements by ultrasound and by histol- one false negative and three false posi-
ogy. This graph shows the reliability of tives, giving a sensitivity of 83%, speci-
ultrasound for evaluation of tumour thick- ficity of 63%, positive predictive value of
ness against histological measurement. The 63% and negative predictive value of
plotted points nearly all lie on a straight 83%.
line, thus showing a very high degree of
correlation (significant at the 0.01 level).
Discussion
Calculation of the Pearson correlation coef-
ficient (r = 0.948, P < 0.01) and the Spear- Most deaths from oral squamous cell
man rank correlation coefficient (r = 0.913, cancer (SCC) occur in association with
P < 0.01) confirm this. The intraclass cor- failure to achieve local or regional dis-
relation coefficient is about 0.95 which ease control11. A smaller percentage of
implies really good reliability. deaths occur as a result of distant meta-
For deep margin clearance, ultrasound static disease. Although many adverse
has good correlation with histology, as prognostic factors are recognised relating
shown by the Pearson correlation coeffi- either to the clinical or histopathological
cient of 0.648 (P < 0.01). The Kappa features of a given tumour, failure to
statistic value of 0.44 shows ultrasound achieve surgical clearance can result in
to have moderate predictive value. local or regional recurrence despite radi-
cal post-op radiotherapy. Achieving sur-
gical clearance is the single prognostic
Table 2. Crosstabulation of histology and factor controlled by the surgeon.
ultrasound detection of close and clear surgi- It is well established that histological
cal margins clearance of 5 mm or more is required in
Histology oral cancer resection in order to reduce
Close Clear Total local recurrence and improve survival10.
In order to achieve 5 mm of histological
Ultrasound Close 5 3 8
– Clear 1 5 6
clearance and to allow for specimen
Total – 6 8 14 shrinkage and surgical error/underesti-
mate9, a margin of 10 mm is advocated
Ultrasound imaging showed sensitivity of
at the time of surgery. Despite this, the
83%, specificity of 63%, positive predictive
value of 63% and negative predictive value of literature shows that approximately 20–
83%. Detection of close and clear surgical 50% of resections are reported histologi-
margins by histology and by ultrasound ima- cally as not clear that is close or involved
ging. Close margin < 5 mm, clear mar- margins19. This is due to underestimation
gin  5 mm. of the true size of the tumour. YUEN
Resection margin by ultrasound 329
et al.24 have shown that even a 10 mm
margin is not safe. They advocate a mini-
mum of 15 mm and a maximum of
20 mm.
A significant proportion of resections
are reported inadequately cleared usually
at the deep margins as this is clinically
difficult to assess. Operatively surgeons
will use two of their sensory faculties,
notably sight and touch, to assess tumour
clearance. However, both of these assess-
ment techniques have significant disad-
vantages. The tumour’s vertical depth of
invasion, like an iceberg, is much more
difficult to assess both pre-operatively
with CT or MRI and clinically at sur-
gery17. It is for this reason that inadequate
resections occur. In order to achieve deep
clearance the thickness of tumour needs to
be known or visualised at the time of
resection. At present, CT and MRI do
not have the resolution to demonstrate
the thickness of primary T1, T2 oral
tumours with certainty6,17. Tumour thick-
ness is an important prognostic factor for
neck metastasis1,4. Furthermore, YUEN
et al.25 reported that tumour thickness is
the only important factor that had signifi-
cant predictive value for subclinical nodal
metastases, local recurrence and survival.
The difficulties of assessing oral
tumours with extra-oral ultrasound mea-
surements in some early studies have now
been overcome by using high resolution
intra-oral probes. More recent studies with
intra-oral ultrasound imaging has been
shown to be useful for evaluating tumour
thickness in tongue carcinoma7,16,17. The
advantages of diagnostic ultrasound are
that it is non-invasive, does not use ionis-
ing radiation, is quick to perform and is
repeatable. The machine is portable and
can be taken to the operating theatre, thus
real time imaging can be carried out at the
time of surgery.
This study sought ways to assess tumour
clearance at the deep margin more objec-
tively by using ultrasound scanning. Our
study demonstrated that depth clearance
can be assessed by ultrasound at the time
of surgery. However, we could only use
ultrasound for tumours on the anterior two
thirds of tongue, floor of mouth and other
regions accessible by the intraoral ultra-
sound probe. Posterior third of tongue
could not be accessed by our ultrasound
probe. The ultrasound measurements
showed a high degree of reliability with
histological measurements for tumour
thickness. For deep margin clearance,
ultrasound had a moderate predictive
value. The discrepancies in deep margin
clearance measurements can be accounted
for by the following reasons:
330 Songra et al.
1. The histology and the ultrasound mea-
surements might not have been made at
exactly the same point.
2. There was some shrinkage of specimen
after resection and after fixation in
formalin.
3. Histological tissue processing took
samples of tissue at the tumour margin,
rather than the whole margin. Thus it
was possible that a tumour with a dee-
ply infiltrating margin at only one point
could be missed on histology.
4. In order to hold the partly resected
specimen in its original position when
the ultrasound measurement was car-
ried out mid-resection, slight compres-
sion at the surface was applied with the
ultrasound probe.
5. There was some additional tissue com-
pression when a metal retractor had to
be placed in the surgical cut in order to
provide an ultrasound reflector.
The study by HELBIG et al.7 assessed the
accuracy of intra-operative ultrasound for
the visualization of tumour size. They only
studied five cases and statistical analysis
was not possible on such small sample.
They used a suture, placed under ultra-
sound guidance, to mark the deep tumour
margin prior to any resection. Whilst this
provided a definitive physical reference
for histological registration of depth, the
method had potential drawbacks such as
tissue distortion and possible interference
with the cells at the margin and ‘‘seeding’’
of tumour cells. HELBIG et al.7 did not a-
ssess surgical margin clearance of tumour.
During the course of our current study
we became aware of the relative ease with
which ultrasound imaging could be
applied to the surface, mucosal margins.
We have carried out a separate study of
this, which will be the subject of a future
publication.
To our knowledge we are the first to
report the use of intraoperative, intra-oral
ultrasound imaging to measure surgical
margin clearance of tumour and to do so
at the time of resection. With the patient
under general anaesthesia, positioning of
the ultrasound probe is easier, particu-
larly if the tumour is posteriorly placed.
There is also less patient movement arte-
fact, leading to more accurate measure-
ment, especially for the tongue. In
addition to making measurements, the
real time nature of ultrasound imaging
lends itself to providing guidance at the
time of surgery. This will have major
impact on surgical practice. If this proves
successful the need for frozen sections
may diminish.
We chose to image the tumour partially
resected but still attached because this
would facilitate interpretation of the ultra-
sound image and give fixed points of refer-
ence. We deliberately did not inform the
surgeon and the pathologist of the ultra-
sound results in order to avoid bias (Haw-
thorn effect). With the pathologist we had
to show them where to cut (or not to cut) the
specimen in order to avoid accidental
damage to the site of interest. Having
obtained encouraging results in this study,
we plan to perform further studies using
ultrasound imaging as an intraoperative
guidance tool, where we will intentionally
influence the surgeon’s actions.
Now that a reliable and accurate tool in
the form of high frequency, high resolu-
tion diagnostic ultrasound is available, it is
possible to objectively assess the surgical
margin and to achieve higher rates of
clearance. The establishment of accurate
tumour thickness measurements will
enable more precise surgery to be per-
formed in the future. This will allow less
mutilating surgery, reduce morbidity and
decrease risks of recurrence.
Conclusion
This original paper shows that high reso-
lution ultrasound imaging, applied intra-
orally to tumours accessible by the ultra-
sound probe, is a good reliable tool in
objectively assessing:
1. tumour thickness;
2. surgical margin clearance at the time of
operation.
Acknowledgements. We are very grateful
to ATL Ltd. for the loan of an HDI 5000
ultrasound machine and to the charity
‘‘The Facial Surgery Research Founda-
tion-Saving Faces’’ and the Special Trus-
tees of Barts and the London NHS Trust
for eventual purchase of this ultrasound
machine. We also thank our Consultant
colleagues Mr. John Carter and Mr. Peter
Hardee in Oral & Maxillofacial Surgery
for permitting access to their patients.
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Address:
Suk Y. Ng
Department of Dental Radiology
Guy’s, King’s and St Thomas’ Dental Institute
King’s College London
Caldecot Road
London SE5 9RW, UK.
E-mail: suk.ng@kcl.ac.uk