ORIGINAL ARTICLE
RECURRENT PLEOMORPHIC ADENOMA OF THE PAROTID
GLAND: ANALYSIS OF 108 CONSECUTIVE PATIENTS
Claus Wittekindt, MD,1 Kristina Streubel,1 Georg Arnold, MD,2 Eberhard Stennert, MD,1
Orlando Guntinas-Lichius, MD1
1
Clinic of Otorhinolaryngology, Head and Neck Surgery, University of Cologne, D-50924 Cologne, Germany.
E-mail: [email protected]
2
Institute of Pathology, Kliniken Essen-Mitte, Essen, Germany
Accepted 5 December 2006
Published online 11 June 2007 in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/hed.20613
Abstract: Background. Surgery for recurrent parotid pleomorphic adenoma is a challenging problem.
Methods. One hundred eight patients who underwent 134
reoperations for recurrent parotid pleomorphic adenoma (followup, 22 years) were evaluated for histopathologic features and
risk factors for recurrence.
Results. The number of reoperations for tumor recurrence
ranged from 1 to 10. Twenty-seven patients (25%) developed
permanent facial nerve weakness. The risks for clinically evident
rerecurrence after 1, 5, and 15 years were 16%, 42%, and 75%,
respectively. Female sex, young age at initial treatment, and
enucleation instead of parotidectomy for treatment of the first
recurrence were significant risk factors for rerecurrence. The
mean number of recurrent tumor nodules was 26.
Conclusions. Surgery for recurrent parotid pleomorphic adenoma has a high rate of facial nerve morbidity. The chance of
rerecurrence is high. Extended parotidectomy seems to be the
best approach for the reoperation to reduce the risk of rerecurC 2007 Wiley Periodicals, Inc. Head Neck 29: 822–828,
rence. V
2007
Keywords: recurrent pleomorphic adenoma; parotid gland; parotidectomy; facial nerve; recurrence
Pleomorphic adenoma is the most common type
of tumor in the parotid gland, making up 60% to
Correspondence to: O. Guntinas-Lichius
C
V
2007 Wiley Periodicals, Inc.
822
Recurrent Pleomorphic Adenoma
70% of all parotid neoplasms.1 It is agreed that
the management of pleomorphic adenoma is imperatively surgical treatment.2 Recurrence rates
of 20% to 45% have been described after simple
enucleation.3,4 The risk of recurrence has been
attributed to the histopathologic features of the
tumor.
It is believed that surgery close to the pseudocapsule increases the risk of incomplete resection
of these microscopic extensions beyond the pseudocapsule or of capsule rupture.5,6 In consequence, wide dissection in the form of superficial
or subtotal parotidectomy was established as
the treatment of choice. Recurrence rates were
thereby reduced to less than 5%.7–9 Despite this
insight, enucleation remains an important risk
factor, especially in cases in which the parotid
tumor was misdiagnosed as a lymph node.2
Treatment of patients with recurrent pleomorphic adenoma is difficult. Indeed, in most cases,
it would be more accurate to speak of residual
disease, since most patients have never been free
of disease. The residual disease just progresses
to a stage at which it is clinically detectable.10
Revision surgery in the parotid area has a higher
morbidity. Particularly, the risk of damaging the
HEAD & NECK—DOI 10.1002/hed
September 2007
facial nerve is high, 15% to 30%, because it is
often well ensheathed in scar tissue with distortion of the local anatomy.11,12
The optimal strategy for a revision surgery
remains controversial because the chance of rerecurrence ranges from 10% to 63%.13–15 Treatment recommendations reach from no treatment
at all to local excision, to radical resection sacrificing the involved facial nerve, or even radiotherapy.2,16–18 Recently, it was shown that most
recurrences are not just multinodular. Microscopically, many recurrences consist of up to 100 nodules or even more. Most nodules are smaller than
1 mm. A large number of nodules are located far
beyond the scar line from prior surgery.19 These
histopathologic features may explain the high
incidence of rerecurrences.
PATIENTS AND METHODS
We reviewed the case records of all patients who
were treated for recurrent pleomorphic adenoma
of the parotid gland at a single center (Clinic of
Otolaryngology, Head and Neck Surgery, University of Cologne, Germany) from July 1974 to April
2004. We identified 108 patients who underwent a
total of 134 operations for recurrent pleomorphic
adenomas of the parotid gland.
The extent of surgery depended on the number
and type of previous surgeries and on the wishes
of the patient. Scar tissue and surrounding subcutaneous tissue was always completely excised at
the beginning of the operation. After lifting the
skin flap, the operations were performed using a
surgical microscope.
Lateral revision parotidectomy was performed
in cases in which recurrent tumor nodules were
localized in the lateral part of the parotid gland.
Subtotal revision parotidectomy was performed in
cases in which the tumor or a part of multiple
tumors were also situated medial to the facial
nerve branches. In all cases, as much periparotid
fat tissue as possible was resected. In cases in
which the facial nerve had previously been
dissected during parotidectomy or the patient had
already undergone repeated interventions, the
recurrent tumor nodules were enucleated together with as much surrounding scar tissue and
remaining parotid tissue as possible without
risking a facial nerve lesion.
But our strategy implied that tumor was never
deliberately left behind in hopes of preserving
nerves. If a thin nerve branch could not be identified, or if conservative excision of nodules medial
Recurrent Pleomorphic Adenoma
to the facial fan was not possible, a radical parotidectomy was performed after the patient provided
informed consent. The respective branch was
typically cut, the tumor was removed, and the
stumps of the nerve branch were then resutured
end-to-end. If an end-to-end nerve anastomosis
was not possible, an interpositional graft with the
greater auricular nerve was performed. Strictly
following the described surgical strategy, macroscopic tumor was not left behind after any of the
revision operations.
Our standardized histopathologic examination
of the tumor nodules was recently published in
detail.19,20 The case records of all patients were
analyzed with regard to type of surgery, facial
nerve dissection, wound defect filling, operation
time, and complications. The facial nerve function
of all patients was registered at discharge. A total
paresis was defined as a complete loss of mimic
muscle function on the affected side without any
signs of voluntary muscle potentials in needle
electromyography. Details on the electromyographic analysis of facial function are given elsewhere.21 A partial paresis was defined as a paresis
of only 1 or several peripheral facial nerve
branches. An isolated paresis of the marginal
mandibular branch was notified separately. Patients with facial weakness were examined clinically and by electromyography every 3 months
after surgery until no further improvement of
facial function could be observed. Additionally,
all patients were instructed to revisit the hospital
in case of a molesting Frey’s syndrome.
Statistical analysis of the data was performed
using SPSS software for medical statistics,
version 11.0.1. Mostly, data are presented as
means 6 SD. The chi-square test was used for
comparison of categorical variables, and the
Mann–Whitney test was used for continuous variables. The Spearman’s rho correlation was used to
analyze the linear relationship of the interval
between 2 operations within the same patients
and histomorphological tumor characteristics.
Recurrence-free survival was calculated by the
Kaplan–Meier product-limit method. All reported
p values are 2-sided. A p value of less than .05 was
considered to be statistically significant.
RESULTS
The study comprised 108 patients, of whom 71
were women (66%) and 37 men (34%). The median age at the moment of initial operation was
34 years (range, 7–75 years). Ninety-four patients
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September 2007
823
(87%) had their initial operation elsewhere. Fourteen patients (13%) underwent their initial operation in our hospital. An enucleation as first treatment was reported for 69 patients (64%), whereas
20 patients (18%) had tumor recurrence develop
after parotidectomy. The extent of the initial
operation was unknown in 19 cases (18%).
The median age at first admission to our
hospital for recurrent pleomorphic adenoma was
49 years (range, 7–93 years). Seventy patients
(65%) were treated for their first and all further
recurrences, and 38 (35%) were treated for later
recurrences or rerecurrences. The patients were
not irradiated elsewhere before or in our institution during the study period.
Overall, 134 reoperations for recurrent pleomorphic adenoma were performed. The type of
reoperation was enucleation in 25 cases (19%),
lateral revision parotidectomy in 35 cases
(26%), total revision parotidectomy in 57 cases
(43%), and radical revision parotidectomy in 9
cases (7%). The type of salvage surgery was
unknown for 8 reoperations (6%). The average
duration of reoperation was 222 6 123 min (range,
30–660 min).
No complications were noted for 100 reoperations (75%). Salivary fistula occurred in 2 cases
(2%), wound infection occurred in 4 cases (3%),
hematoma was present in 9 cases (7%). No data
about perioperative complications were available
for 19 reoperations (14%). Normal facial nerve
function was noted at discharge for 59 operations
(44%). After 43 operations (32%), a paresis of the
marginal mandibular branch of the facial nerve
was noted. In 9 cases (7%), a partial paresis was
documented, and in 16 cases (12%), a total facial
nerve paresis was documented. The facial nerve
status at discharge was unknown in 7 cases (5%).
The risk of a perioperative facial nerve paresis was
higher after subtotal revision parotidectomy than
after a less extended revision operation (p ¼ .048).
Details for long-term sequelae were available
for 94 cases (87%). Fifty-six patients had no longterm sequelae (52%), whereas 18 patients (16%)
had permanent facial nerve weakness development. A permanent complete paresis did not occur.
The risk for a permanent facial paresis did not
depend significantly on the chosen type of revision
surgery (p ¼ .553). The facial nerve repair in 9
patients resulted in House-Brackmann facial
function grade 2 in 1 patient, grade 3 in 6 patients,
and grade 4 in 2 patients. A Frey’s syndrome that
needed treatment with botulinum toxin type A
occurred in 11 patients (9%).
824
Recurrent Pleomorphic Adenoma
The histopathologic examinations on serial
sections revealed multinodular lesions in 111 cases
(83%), whereas uninodular recurrence was present in 17 cases (13%). The number of nodules
was unknown in 6 cases (5%). The mean number
of tumor nodules was 26 6 41 (range, 1–266).
The median follow-up time in relation to the
primary operation was 19.3 years (range, 2.3–
53.8 years). The median follow-up time after most
recent reoperation was 7.4 years (range, 0–18.8
years). Figure 1 gives an overview about reoperation characteristics and recurrence rates. Thirtytwo patients (30%) had 1 single recurrence and
are to date clinically free of the disease. Fifty-six
patients (52%) had further rerecurrences develop.
Twenty patients (19%) had an unknown outcome.
The mean number of reoperations for tumor
recurrence in each patient was 2 6 1.7 (range, 1–
10). The mean interval between reoperations was
7.2 6 6.9 years (range, 0.02–33.4 years). No correlation was seen between the time interval
between the initial operation and first reoperation
and the number of tumor nodules (Spearman’s
rho correlation r ¼ .017; p ¼ .855). Additionally,
the time interval to any previous reoperation did
not show an influence on the number of pleomorphic adenoma nodules (Spearman’s rho correlation r ¼ .056; p ¼ .545).
Information about the actual clinical status
was available for 74 patients (69%). Forty-nine
patients (45%) were clinically relapse-free, and 25
patients (23%) lived with a recurrent tumor.
According to the Kaplan–Meier method, the chances of a second recurrence after 1, 2, 5, 10, and 15
years were 16%, 23%, 42%, 60%, and 75%,
respectively. Regarding the last operation, the
chances of further rerecurrence after 1, 2, 5, 10,
and 15 years were 16%, 19%, 31%, 47%, and
52%, respectively.
Numerous clinical variables were assessed as
potential risk factors for parotid pleomorphic adenoma recurrence (Tables 1 and 2). The type of the
initial operation (enucleation vs parotidectomy)
showed no significant influence on the time interval between initial operation and first reoperation
(p ¼ .182), the frequency of recurrences (single vs
multiple recurrences; p ¼ .433), or the overall control rates (p ¼ .078).
The rate of multiple recurrences was significantly higher in female patients (p ¼ .01) and in
younger patients (p < .001). The type of first reoperation influenced the risk of further rerecurrences in the group of patients who were treated
for all recurrences and in patients who were
HEAD & NECK—DOI 10.1002/hed
September 2007
FIGURE 1. Schedule of 108 patients undergoing 134 operations for recurrent parotid pleomorphic adenoma. The proportions of
patients with single versus multiple recurrences are shown.
treated for later recurrences and rerecurrences,
respectively. More rerecurrences were seen with
patients treated by enucleation than with those
treated by lateral or subtotal revision parotidectomy (p ¼ .039). If we consider only the patients
who have undergone surgery for further recurrence in our department (n ¼ 70), the effect is
even more significant (p ¼ .017). The interval
between initial surgery and first reoperation did
not influence the number of further rerecurrences
(p ¼ .368). Histopathologic characteristics of recurrent pleomorphic adenoma nodules after first
revision surgery for recurrence did not influence
the risk of rerecurrence (Table 2).
DISCUSSION
Pleomorphic adenoma is generally solitary at initial presentation. A strong relationship exists
between initial surgical technique and recurrence
rate.22 Enucleation yields the highest recurrence
rates, whereas parotidectomy is associated with
low recurrence rates.23,24 Local recurrence will
occur in at least one third of the patients who
Table 1. Relation between patients’ and operation characteristics and the risk of rerecurrence.
Characteristic
Sex
Female
Male
Age at first operation in years
(mean 6 SD)
Interval between initial surgery and
first reoperation in years (mean 6 SD)
Type of initial surgery
Unknown
Enucleation
Parotidectomy
Type of first reoperation
Unknown
Enucleation
Lateral parotidectomy
Subtotal parotidectomy
Radical parotidectomy
Recurrent Pleomorphic Adenoma
All patients
(N ¼ 108)
Status
unknown
(n ¼ 20)
Single
recurrence
(n ¼ 32)
Multiple
recurrences
(n ¼ 56)
71
37
34.9 6 14.1
9
11
39.1 6 18.7
18
14
40.3 6 11.3
44
12
30.2 6 12.2
<.0001
9.1 6 7.5
7.7 6 6.8
10.5 6 7.9
8.9 6 7.6
.368
19
69
20
3
12
5
3
24
5
13
33
10
8
13
33
52
2
4
2
9
5
0
0
2
9
21
0
4
9
15
26
2
p value
.01
.433
.039
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September 2007
825
Table 2. Relation between the histopathologic characteristics at first reoperation for parotid pleomorphic adenoma
and the risk of rerecurrence.
Histopathologic findings
at first reoperation
All patients
(N ¼ 108)
Status unknown
(n ¼ 20)
Single recurrence
(n ¼ 32)
Multiple
recurrences
(n ¼ 56)
p value
Number of nodules
(mean 6 SD)
Nodule size in mm
(mean 6 SD)
Nodules <1 mm
Unknown
Yes
No
Histologic subtype
Unknown
Predominately myxoid
Not predominately myxoid
Encapsulation
Unknown
Focally absent
Circular present
Nodules outside scar
Unknown
Yes
No
28.1 6 41.1
24.2 6 36.9
40.8 6 56.9
22.5 6 29.5
.336
19.1 6 13.9
22.8 6 15.2
17.9 6 8.7
18.5 6 15.8
.191
.453
42
52
14
6
10
4
10
17
5
26
25
5
33
58
17
6
9
5
8
19
5
19
30
7
35
39
21
9
4
2
7
15
7
19
20
12
36
59
13
9
6
5
7
21
3
20
32
5
.650
.166
.061
undergo enucleation.25,26 If the tumor is violated
during enucleation, multiple new tumors may
slowly start to grow in the surgical field. The
result would be a seeding of multiple new nodules
in the area of operation and also beyond the scar
line in untouched tissue.5 This has been shown in
a recent histopathologic analysis in serial sections20 and was confirmed by the present examination: the mean number of nodules was 26, and
the maximal number was 266. When a patient
presents with a recurrent pleomorphic adenoma,
the number of nodules is probably much higher
than is clinically evident or even detectable by
modern MRI.27 Therefore, a surgical technique is
strictly demanded with removal of tumor with as
much normal surrounding gland tissue as possible. Hence, it is conclusive that in our series
extended revision parotidectomy compared with
simple enucleation of clinically visible tumors significantly reduced the probability of rerecurrence.
Half of all patients in our series had a rerecurrence develop. Lower rates from 11% to 18% are
published in other series.15,18 The probability for
a second recurrence after 10 years was 60%, and
for further recurrences was 47%. Comparable
values in the literature range from 20% to 40%
for a second recurrence and 20% for further recurrences.15,18 The higher recurrence rates in our
826
Recurrent Pleomorphic Adenoma
series simply could be attributed to the rigid
schedule of routine follow-up examinations.
Revision surgery is accompanied by a higher
risk of permanent facial nerve weakness than primary surgery.2,18 Only if the initial surgery was
enucleation without exposure of the facial nerve,
following revision parotidectomy could be performed without enhanced risk for the facial nerve.
We found that a quarter of all patients in our
series suffered from some degree of permanent
facial weakness. However, the risk was independent of the extent of the revision surgery procedure.
We believe that our standardized surgical strategy is the reason why even extended subtotal
revision parotidectomy was not more likely to
predispose to nerve injury. The procedure is time
consuming. In the present series, the average
time was over 4 hours. This procedure is worthwhile because it decreases the risk of rerecurrence
significantly. Moreover, despite our policy to
attempt to extend the area of resection as much as
possible, we did not observe a higher rate of permanent facial paresis than in other series.2,11,28
Young and female patients were by far overrepresented in our study. Younger age as risk factor
was also quoted in another series.10 Presumably,
surgeons tend to provide these patients with small
skin incisions. In the elderly, tumor recurrence
HEAD & NECK—DOI 10.1002/hed
September 2007
frequently is not noted before the patients die or
the small growth of clinically evident recurrence
leads the physicians to advise their patients to a
‘‘wait and see’’ strategy. Therefore, time between
the first operation and recurrence varies between
1 and 10 years after initial surgery in most studies
as well as in the present study.11,29 The intervals
between recurrences decreased with later recurrences, probably because the patients were
revisited more often. There were no cases of malignant degeneration. In another large study of
114 patients, some cases with malignant degeneration were seen.18 It may be concluded that malignant transformation is rarer in recurrent tumors
than in primary parotid pleomorphic adenoma
with long history before operation. The role of
adjuvant radiotherapy remains controversial in
recurrent pleomorphic adenoma. No study exists
to date that compares surgery versus surgery
combined with radiotherapy or radiotherapy
alone. However, it should be noted that it is difficult to justify irradiating in an attempt to prevent
recurrence of a benign tumor in a collective with
many young patients as a rescue for inadequate
surgery in primary as well as in recurrent pleomorphic adenoma. Since radiotherapy has been
reported to improve local control in patients with
multinodular recurrence, immediate adjuvant
radiotherapy might be appropriate when a residual tumor or massive spillage at revision surgery
is documented.14,18
Acknowledgment. Dr. J. Vent is gratefully
acknowledged for critical reading of the paper.
The clinical and histopathologic analysis of 108
patients with recurrent pleomorphic adenoma
showed the dangerous features of the recurrent
tumor nodules and the multicentricity of the
disease leading to high rerecurrence rates and
considering morbidity of the facial nerve. The
detailed risk analysis revealed that females and
young people showed a higher risk for the development of recurrence. If possible, extended parotidectomy is the method of choice for salvage surgery
of recurrent pleomorphic adenoma. This procedure seems to reduce the risk of rerecurrence. The
expectations from a reoperation should be critically proven. Not the presence of recurrence
alone, but rather the presence of symptoms or disease location that implies significant morbidity
overtime if left to grow unchecked are indications
for a reoperation that outweigh the high potential
of morbidity after reoperation.
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