J Oral Maxillofac Surg

.56:814-820, 1998

Surgical Treatment of Squamous Cell

Carcinoma of the Lower Lip: Evahation of
Long-Term Rem&s and Prognostic Factors-
A Retrospective At&y& of l&i Patients
Jan G.A.M. de Visscher, DDS, MD, * Karin uan den Elsaker, f
A. Joris K. Grand, MD, PbD,# Jacqueline E. van der Wal, DDS, MD, PbD,$
and Isa& van der Waal, DDS, PhDlj

Purpose: A retrospective study was undertaken to evaluate the results of surgical treatment of primary
squamous cell carcinoma of the vermilion border of the lower lip and to identify parameters of the
primary tumor that may predict local recurrence and regional metastasis.
Patients From 1979 through 1992, 184 consecutive patients with a primary squamous cell
and Methods:
carcinoma of the lower lip underwent surgical excision as a primary treatment. There were 166 (90.2%) men and
18 (9.8%) women, with a mean age of 66 years. Most cases(92.9%) were stage I tumors. Most of the tumors were
well and moderately differentiated squamous cell carcinomas (93.5%). Minimal follow-up was 2 years, with a
mean of 56 months. Disease control was achieved in 165 (89.7%) patients. Local recurrence and regional
metastasis occurred in 9 (4.9%) and 10 (5.4%) patients, respectively. Local failures were treated successfully by
either surgery or radiation therapy. Regional metastases were treated in nine patients by neck dissection,
followed in eight casesby radiation therapy. One patient developed distant metastasis.
Results: Five- and 1syea.r overall survival rates were 78% and 6l%, respectively, whereas the disease-free
survival rates at 5 and 10 years were 86% and 81%, respectively. Multivariate analysis indicated that local
recurrence was signiticantly associated with large tumor size and surgical margins containing squamous cell
carcinoma. Increasing tumor thickness, an infiltrative invasion pattern, and perineural invasion were significant
prognostic indicators of regional metastasis.
Conclusion: Surgical treatment for small squamous cell carcinomas of the lower lip has a favorable
prognosis. Particular parameters of the primary tumor seem to predict the chance of development of local
recurrence and regional lymph node metastasis.

*Oral and Maxillofacial Surgeon, Department of Oral and Maxillo- Most cancers of the vermilion border of the lip are
facial Surgery, Medisch Centrum Leeuwarden, The Netherlands. squamous cell carcinoma (SCC), occurring most fre-
tData Manager, Radiotherapeutic Institute Friesland, Leeuwar- quently on the lower lip. Surgery and radiation therapy
den, The Netherlands. are the principal modalities used in treatment of lip
*Pathologist, Department of Pathology, Laboratory of Public cancer. SCC of the lower lip carries a good prognosis,
Health Friesland, Leeuwarden, The Netherlands. which is attributed to early detection and the rela-
§Associate Professor, Department of Oral and MaxiUofaciaL Sur- tively infrequent occurrence of regional metastasis.
gery/Pathology, Free University Hospital/ACTA, Amsterdam, The However, death of lip cancer still occurs.
Netherlands. The prognosis for cure varies depending on the
[IProfessor and Chairman, Department of Oral and Maxillofacial extent of the disease at the time of presentation. The
Surgery/Pathology, Free University Hospital/ACTA, Amsterdam, 5-year determinant survival rates for Tl and T2 tu-
The Netherlands. mors, without evidence of regional lymph node in-
Address correspondence and reprint requests to Dr de Visscher: volvement, range from 85% to 99% and from 71% to
Department of Oral and Maxillofacial Surgery, Medisch Centrum Leeu- 97%, respectively, irrespective of the treatment modal-
warden, Henri Dunantweg 2,8934 AD Leeuwarden, The Netherlands. ity.ib However, in some studies, it has been shown
o 1998 American Association of Oral and hbxillofacial Surgeons that surgery for these tumors is more effective than
0278.2391/98/56070002$3.00/0 radiation therapy.6,7 Advanced tumors, T3 and T4

814
de VISSCHER ET AL
lesions, and those with lymph node involvement, are
generally treated by a combination of the two treat-
ment modalities. The 5-year determinate survival rates
range from 40% to 80%.‘-*s6
The most powerful predictor of survival is the
presence or absence of cervical lymph node metasta-
ses. Because lower lip cancers, irrespective of their
size, may metastasize, it is important to detect those
patients with tumors with a high propensity of nodal
metastasis. The current retrospective study was under-
taken to evaluate the results of surgical treatment of
primary SCC of the vermilion border of the lower lip
and to identify clinical and histologic parameters of
the primary tumor that may predict local recurrence
and regional lymph node metastasis.
Patients and Methods
From 1979 through 1992, 184 consecutive patients
with a primary, solitary SCC of the vermilion border of
the lower lip (International Classification of Diseases
for Oncology [ICD-01 140.1) who were treated by
surgical excision as the primary form of treatment,
were retrospectively reviewed. The preference for
number
30
25
20
15
10
0 II
<40 40-44 45-49 50-54
FIGURE 1. Distribution of 184 patients with SCC
81.5
surgery versus radiation therapy as the treatment
modality for lip cancer had not specifically been
defined in that period.
DEMOGRAPHIC CHARACTERISTICS
The patient data were retrieved from the medical
records at four hospitals in the County of Friesland
(n = 162) and from the medical records at the Depart-
ment of Oral and Maxillofacial Surgery of the Free
University Hospital of Amsterdam (n = 22). Figure 1
shows the age and gender distribution of the patients
involved in the study. There were 166 (90.2%) males
and 18 (9.8%) females. The mean age was 66 years
(range, 32 to 98). All patients were white.
STAGEAND TREATMENTCHARACTERISTICS
The following clinical information was obtained
from the medical records: site, stage of the disease
according to the TNM classification,s initial treatment,
local recurrence, metastasis, treatment of local recur-
rence and regional metastasis, and development of
second primary tumors on the lower lip.
There were 87 (47.3%) left-side, 69 (37.5%) right-
. . . _ __ _
... ...... ..
55-59 60-64 65-69 70-74 75-79 60-64 85-90 >90
age
of the lower lip by age and gender.
816
NO Nl N2 Total
Tl 170 1 171
T2 9 1 10
T3 1 1
T4 1 2
Total 179 : 1 184
side, and 28 (15.2%) middle third of the lip lesions.
The distribution of clinical T and N stages on presenta-
tion is shown in Table 1. Most of the patients (92.9%)
presented with stage I lesions. At the time of the initial
physical examination, five patients had palpable cervi-
cal lymph nodes at level I. These clinically suspicious
lymph nodes were not examined preoperatively by
fine-needle aspiration cytology.
Surgical treatment for the primary tumor consisted
of a full-thickness V- or W-shaped excision and pri-
mary closure in 166 (90.2%) patients. Five had a
non-full-thickness excision, whereas the remainder
had large surgical excisions that were reconstructed
with local flaps. Nine patients underwent a neck
dissection, simultaneous with the initial excision of
the lip tumor, which was a bilateral neck in five
patients.
HISTOLOGY
The histologic specimens of the primary tumor
were reviewed without additional clinical informa-
tion. Histologic criteria evaluated were tumor grade
(well, moderately, poorly, or undifferentiated), surgi-
cal margin status (positive, dysplastic, or negative),
tumor thickness (measured by an ocular grid), growth
pattern (endophytic or exophytic), invasion pattern
(pushing or infiltrative borders), host response (immu-
noreactive cell infiltrate in the tumor-surrounding
stroma defined as either scanty, moderate, or intense),
perineural invasion, and vessel invasion.
Though some specimens did not allow reliable
scoring (registered as unknown), all data of those
patients experiencing local recurrence and regional
metastasis were available. Most of the tumors were
well and moderately differentiated SCCs (93.5%);
there were no undifferentiated tumors. Venous inva-
sion was found in one specimen. Lymphatic vessel
invasion was not observed in any specimen.
Tumor-free resection margins were found in 154
(83.7%) patients, 22 (12%) patients had surgical mar-
gins containing dysplasia, and eight (4.3%) patients
had margins positive for SCC. In none of the patients
with surgical margins containing either KC or dyspla-
sia was additional treatment performed immediately.
Microscopic examination of the nine neck dissec-
LOWER LIP SQUAMOUS CELL CARCINOMA
tion specimens revealed cervical lymph node metasta-
ses in two patients (cTlN1; cT2NO). Thus, of five
patients with clinically assessed lymphadenopathy,
only one had histologically confirmed lymph node
involvement.
CLINICAL OUTCOME: LOCAL RECURRENCE,
SECOND PRIMARIES,LYMPH NODE METASTASIS
Minimal follow-up was 2 years, unless patients died
of their disease. Recurrent disease was defined as
tumor growth at the same site within 5 years after
completion of initial therapy. SCC arising at another
site on the lower lip or after this 5-year period at the
site of the initial tumor were regarded as second
primary malignancy.
Local recurrence was observed in nine (4.9%)
patients, all cTlN0 cases, after a mean follow-up of 38
months (range, 8 to 58 months). These failures were
controlled by local excision in five patients and by
local radiation therapy in four patients. The mean
follow-up of these patients after salvage treatment was
51 months (range, 10 to 84 months). Sixteen months
after radiation therapy, one of these patients devel-
oped a submental lymph node metastasis that was
treated by neck dissection and radiation therapy
(follow-up, 80 months).
Of the eight patients with positive surgical margins
(mean follow-up, 56; range, 10 to 108 months), three
developed recurrent disease after 58, 72, and 82
months, respectively. Of the 22 patients with dyspla-
sia at the surgical margins (mean follow-up, 58; range,
28 to 137 months), none developed a recurrence.
However, in two of the latter patients, a second
primary tumor, located elsewhere on the lip, was
observed after 11 and 39 months, respectively.
Second primary lip SCCs were observed in six
(3.3%) patients. In five patients, second primary tu-
mors were located elsewhere on the lower lip. In the
remaining patient, the second primary tumor was
located at the site of the initial tumor and occurred 72
months after initial treatment. Because the surgical
margins of the first tumor were free of tumor or
dysplasia, this was considered a second primary le-
sion. The interval between the independent carcino-
mas varied from 11 to 78 months (mean, 54 months).
All tumors were controlled by surgical excision.
Cervical lymph node metastases occurred metachro-
nously in 10 (5.4%) patients (nine cTlN0, one cT2NO)
at a mean follow-up of 26 months (range, 7 to 100
months). Nine patients with regional metastases in
level I underwent a neck dissection, which was
followed in eight cases by radiation therapy, with a
total tumor dose of 60 Gy. One patient with clinical
lymph node involvement at levels I to III received
induction chemotherapy before radiation therapy (70
Gy), followed by salvage neck dissection. He died of
de VISSCHER ET AL
complications of treatment after 2 months. One pa-
tient with regional metastasis observed 100 months
after initial surgery of a cT2NO tumor was treated by
salvage neck dissection and radiation therapy. The
patient died 7 months after completion of therapy,
and autopsy showed pulmonary and generalized bone
metastases. Another patient died 8 months after sal-
vage treatment, of a heart attack, without clinical
evidence of recurrent disease. The remaining seven
patients were cured definitively (mean, 76 months;
range, 22 to 125 months). Microscopic assessment of
the 10 neck dissection specimens showed extranodal
metastatic disease in five patients.
SURVIVAL
Overall survival (OS) was defined as the interval
between the date of surgery and the date of last
consultation or date of death due to any cause.
Disease-free survival (DFS) was calculated from the
date of surgery until diagnosis of the first recurrence
or metastasis. For patients who never had a recur-
rence, DFS coincided with OS.
The mean follow-up from initiation of surgery was
56 months, with a range of 2 (including those patients
who died of the disease, during treatment, or of an
unrelated cause) to 166 months.
STATISTICALANALYSIS
Actuarial survival and disease-free rates were calcu-
lated using the Berkson-Gage lifetable method. To
determine the potential prognostic value of clinical
and histologic parameters for their relation to the
likelihood of local recurrence and metastasis, statisti-
cal analysis of the results was done using the x2 test for
univariate analysis and the logistic regression model
for multivariate analysis. The data were analyzed with
the SPSSprogram (SPSSInc., Chicago, IL). The values
were considered to be significant at P IS .05.
FIGURE 2. Overall and disease-free sur- z
viva1 curves according to Berkson-Gage 5 0.7
among 184 patients with primary SCC of ‘F
the lower lip in relation to response to g
surgery. 9 0.6
a
817
Results
At the end of the study period, 135 (73.4%) patients
were alive and clinically free of disease. Of the
patients who had died, most died of advanced age; a
single (0.5%) patient died as a result of lip cancer, one
died during lip cancer treatment, and 11 died of
subsequent unrelated cancers. Immediate disease con-
trol was achieved in 165 (89.7%) of the patients.
For the entire group, the actuarial overall survival
rates at 5 and 10 years were 78% and 6l%, respec-
tively, whereas the cumulative disease-free survival
rates at 5 and 10 years were 86% and 81%, respectively
(Fig 2).
Table 2 shows the correlation between the studied
variables and recurrence and metastasis. Univariate
analysis results of the independent correlation be-
tween clinical and histologic variables and recurrence
and metastasis are summarized in Table 3. Multivariate
analysis showed that local recurrence was statistically
significantly associated with large tumor size (P < .Ol)
and surgical margins containing SCC (P = .02),
whereas regional metastasis was strongly associated
with increasing tumor thickness (P < .OOl), an infiltra-
tive invasion pattern (P = .04) versus pushing borders
and perineural invasion (P = .05).
Discussion
The demographic, clinical, and histologic features
of the patients with cancer of the lip in this study were
similar to those of others using surgery or radiation
therapy for cure. 16,9-1
l Most of the patients were aging
men and had small tumors and a low incidence of
cervical nodal disease at presentation. Furthermore,
the 5- and lo-year cumulative disease-free rates in this
series were comparable to those reported in other
studies.
-0SC +DFSC
818 LOWER LIP SQUAMOUSCELL CARCINOMA

The histologic margin status is reported to have a

significant influence on local recurrence, whereby
positive margins show a high recurrence rate if they
are not retreated promptly.7~10J2 Safe margins, includ-
No. of Recurrence Metastasis ing a zone of adjacent normal tissue preferably not less
Variables Patients (%) cw cm than 1 cm, are recommended,4J3 although 3 to 5 mm
Age (v-1 seems to be sufticient.14J5 The use of intraoperative
30-39 5 (2.7) - - frozen sections may reduce the number of patients in
40-49 12 (6.5) - 8.3 whom microscopically positive margins are present.
50-59 37 (20.1) - 5.4 The issue of whether to perform additional treatment
60-69 49 (26.6) 10.2 6.1
6.0 8.0 when the margins show dysplasia is a matter of
70-79 50 (27.2)
80+ 31 (16.9) 3.2 - debate. In the current study, no local recurrent
Gender disease was observed in any of the patients with
Male 166 (90.2) 4.2 5.4 surgical margins containing dysplasia.
Female 18 (9.8) 11.1 5.6 Patients with lower lip cancer tend to develop
Size(mm)
- - second primary SCCs in an average time of 10 years.16
1-5 16 (8.7)
6-10 85 (46.2) 4.0 3.0 In actinic cheilitis, the vermilion border may appear
11-15 42 (22.8) 3.6 14.3 clinically irmocuous, although, at a microscopic level,
16-20 18 (9.8) 33.3 16.7 it may harbor morphologic changes ranging from
>20 13 (7.1) - 10.0 hyperkeratosis to SCC.l7 Therefore, treatment of the
Unknown 10 (5.4) - -
entire lip has been recommended to prevent develop-
Grade
Well 79 (43) 5.1 3.8 ment of secondary primary cancers.5
Moderately 93 (50.5) 4.3 6.5 In this series, the rate of regional metastases was
Poorly 10 (5.4) 10.0 10.0 within the reported range of other series and varied
Unknown 2 (1.1) - -
between 0% and 15% for Tl tumors, between 11% and
Margin status
35% for T2 tumors, and between 17% and 100% for T3
Clear 154 (83.7) 3.9 5.8
Dysplasia 22 (12) - - and T4 lesions.2J0Js-20 The presence, extent, and
see 8 (4.3) 37.5 12.5 management of regional lymph node involvement
Thickness (mm) seem to be the most important prognostic determi-
1-3 105 (57.1) 4.8 1.9 nants for survival. Except with large nodes, palpation
4-5 40 (21.7) 2.5 5.0 of the neck has been shown to be unreliable in the
6-t 23 (12.5) 13.0 26.1
unknown 16 (8.7) - - evaluation of the extent of the disease for head and
Growth pattern neck SCCS.*~~~~ The presence of clinically synchro-
Endofytic 139 (75.6) 4.3 5.8 nous enlarged regional lymph nodes associated with
Exofytic 33 (17.9) 9.1 6.1 lip cancer does not always correlate with the presence
unknown 12 (6.5) - -
of actual tumor metastasis. Although in this study five
Invasion pattern
Pushing 132 (71.7) 6.1 3.8 (2.7%) patients initially had clinically positive regional
Infiltrative 34 (18.5) 2.9 14.7 lymph nodes, only one had histologically proven
unknown 18 (9.8) - -
Host response
Scanty 6 (3.3) 50.0 16.7
Moderate 24 (13) 4.2 8.3
Intense 137 (74.5) 3.6 5.1
Unknown 17 (9.2) - -
Perineural invasion
Absent 169 (91.9) 4.1 4.1
20.0 30.0 Parameters Recurrence Metastasis
Present 10 (5.4)
Unknown 5 (2.7) - -
Age NS NS
Recurrence Gender NS NS
Absent 175 (95.1) 4.0 NS
Size <.Ol
Present 9 (4.9) 33.3 Grade NS NS
Margin status <.OOl NS
Thickness NS COO1
Growth pattern NS NS
Retrospective studies, such as the current one, have Invasion pattern NS =.02
their limitations. However, some conclusions can be Host response <.OOl NS
drawn from the results of this study. Our multivariate Perineural invasion =.03 COO1

analysis data show that surgical margin status and Recurrence C.001

large tumor size are predictors of local recurrence. Abbreviation: NS, not significant.
de VISSCHER ET AL 819

evidence of lymph node involvement. Indeed, the sponse in predicting lymph node metastasis is un-
rates of clinically false-positive node involvement clear. Although an inverse relationship between the
seem to be high for lip carcinoma, varying from 41% degree of inflammatory response and metastasis has
to 79%.00x23-25 been observed, it was not apparent that the nonspe-
The issue of whether to perform elective neck cific immune surveillance serves as a parameter of
dissection as part of the primary therapy for cancer of node metastasis.31 However, results of studies are
the lip has been debated for years. This subject variable in this respect.34,35
remains a matter of controversy and is determined by Accurate histologic analysis seems to be of major
the reduced survival rates after treatment of metachro- importance because several of the aforementioned
nous cervical lymph node metastases with reported parameters may aid in making therapeutic decisions
mortality rates up to 90%.24JG29 However, in the and improving survival rates. However, it is important
current study and other series,30,31 these adverse to emphasize that the relative importance of the
results were not observed. Elective neck dissection for various independent factors and the quantitative inter-
‘I1 and T2 lesions shows a low rate of histologically- relation between each of them to predict the chance
proven nodal metastasis.25,32 Therefore, the decision of development of nodal disease may be difficult to
of whether to perform elective treatment of the neck assess.Analysis of the data of this study and the results
should be determined by the risk of occult nodal of others suggest that elective neck dissection may be
disease. Previously reported data and the results of indicated in advanced tumors, lesions greater than 6
this study indicate that various clinical and histologic mm in depth, and those with an invasive growth
features of the primary tumor may predict the biologic pattern, perineural invasion, and local recurrence. It
behavior of the tumor and therefore may be useful also may be indicated in patients in whom follow-up is
criteria for selecting high-risk patients. not warranted.
A close relationship between tumor size and the Although most regional metastases occur within the
incidence of cervical lymph node metastasis has been first 3 years after treatment, the incidence increases
reported.3,4,6J0 Furthermore, the degree of histologic with duration of follow-up irrespective of treatment
differentiation has been shown to have a significant modality, whereby 95% of all metastases take place
influence on the occurrence of metastasis.4J0s33-35 within 5 years after treatment.i2 For that reason, a
Maximum tumor thickness has also been recognized follow-up of at least 5 years is recommended.
as a valid parameter in predicting lymph node metasta-
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Discussion
Surgical Treatment of Squamous Cell
Carcinoma of the lower lip: Evaluation
of Long-Term Results and Pro nostic
Factors -A Retrospective Ana f ysis of 184
Patients
Randall M. Wilk, DDS, PhD, MD
Assistant Professor, Department of Oral and Maxillofacial
University of Medicine and Dentistry of NewJersey, NewJersey
Dental School, Newark, NewJersey
This article by devisscher et ai reports on a retrospective
study of lower lip squamous cell carcinomas treated initially
with surgery over a 13-year period. The intent was to
identify parameters of the primary tumor that would predict
local recurrence and regional metastasis. One hundred
eighty-four patients were included in the study, and most
cases were stage I tumors (92.9%) that were weil differenti-
ated (93.5%), which is consistent with other studies of iip
cancer.l~z
The most potent predictor of survival for head and neck
cancer is the occurrence of cervical lymph node metastasis,
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39. Taban SR, Stem AL: Augiogenesis in invasive squamous cell
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metastatic risk. J Cutan Path01 22:236, 1995
and the lip is no exception. Delineating factors that predict
the biologic behavior of any given tumor can certainly
impact on survival and alter treatment.
The surgical procedures in this study consisted of fuli-
thickness excisions in 90.2%, with the remainder having
superficial excisions. No mention is made about vermilionec-
tomy (lip shave) in addition to excision of the lesion in any
of these patients. For actinicaily damaged lips, many sur-
geons advocate a lip shave along with a full-thickness wedge
Surgery,
excision.
Positive surgical margins were also implicated as a prog-
nostic indicator for recurrence. At the time of discovery of
the positive margins, no further treatment was rendered
(either further surgery or radiation therapy) until recurrence
was noted. Three of the eight patients with resections in this
study who showed positive surgical margins went on to
develop recurrences. Re-excision or radiation therapy, in
light of the finding of positive margins, would be more
prudent than a watch-and-wait position. Five of the eight
patients with positive margins had no sequelae.
The issue of elective neck dissection remains controver-
sial. Nine patients in this study underwent neck dissection,
five of them for clinically positive nodes. Only one of the five