Vol. 117 No. 6 June 2014
Pleomorphic adenoma and benign parotid tumors: extracapsular dissection vs superficial parotidectomydreview of literature and meta-analysis Enrico Foresta, MD,a Andrea Torroni, MD, PhD,a Francesco Di Nardo, MD,b Chiara de Waure, MD,b Andrea Poscia, MD,b Giulio Gasparini, MD,a Tito Matteo Marianetti, MD,a and Sandro Pelo, MDa Complesso Integrato Columbus, Catholic University Medical School, Rome, Italy; Institute of Nuclear Medicine, Catholic University of the Sacred Heart, Rome, Italy
Objective. This study compared extracapsular dissection (ED) vs superficial parotidectomy (SP) in the treatment of pleomorphic adenoma and benign parotid tumors. Study Design. The research covered the years 1950-2011 in PubMed, Ovid MEDLINE, the Cochrane Database of Systematic Reviews, and Scopus. Of 1152 articles screened, 123 studies met the inclusion criteria. A review of the nomenclature of the different parotid surgery techniques was done. Recurrence rate, permanent facial nerve paralysis, and Frey syndrome of patients who underwent ED vs those who underwent SP were compared by meta-analysis. Results. Our meta-analysis data comparing ED and SP found that: (1) the recurrence rate is higher in patients treated with SP; (2) SP has a higher incidence of cranial nerve VII paralysis; and (3) Frey syndrome is more common after SP. Conclusions. ED may be a viable option in the treatment of unilateral benign parotid tumors of the superficial lobe, sized less than 4 cm, without involvement of the facial nerve. (Oral Surg Oral Med Oral Pathol Oral Radiol 2014;117:663-676)
Tumors of the salivary glands represent 3% to 10% of all head and neck neoplasms1-15; 75% to 85% of them originate in the parotid gland, and 70% to 80% are benign. Most involve the superficial lobe of the parotid, which accounts for 80% of the gland parenchyma.8,16-29 The most common benign tumors of the parotid gland are pleomorphic adenoma and Warthin tumor. Pleomorphic adenomas lack a complete capsule and are surrounded by healthy gland tissue, which is compressed as they grow. They often present with very small outgrowths extending to the adjacent tissue. It is commonly believed that this histologic feature accounts for their clinical behavior, multicentricity, and recurrence over time.1-3,11,14,21,24-30 The close relationship between the gland and the facial nerve, as well as the high recurrence rate, has shaped surgical techniques for parotid gland neoplasms over the years.17 Enucleation was first described by Senn7 in 1895 as the surgical technique of choice. It was not accompanied by facial nerve dissection. Removal of the tumor was incomplete, as there was tissue left behind. This procedure was widely used in parotid gland tumors for 30 years. In 1921, Sistrunk modified this technique, adding retrograde dissection of a
Maxillo-Facial Surgery, Complesso Integrato Columbus, Catholic University Medical School. b Institute of Nuclear Medicine, Catholic University of the Sacred Heart. Received for publication Jun 7, 2013; returned for revision Feb 11, 2014; accepted for publication Feb 18, 2014. Ó 2014 Elsevier Inc. All rights reserved. 2212-4403/$ - see front matter http://dx.doi.org/10.1016/j.oooo.2014.02.026
the mandibular branch of the facial nerve.8 The treatment of parotid pleomorphic adenoma remained substantially unsuccessful until 1940, owing to a high recurrence rate (45%) and facial nerve paralysis,3,5,6,31 prompting more in-depth microscopic studies of pleomorphic adenomas and modifications of surgical techniques. In 1940, Janes9 published his first article on salivary gland tumor surgery by parotidectomy with dissection and preservation of the main trunk and branches of the facial nerve. In this procedure, the whole superficial lobe was removed along with the tumor. In 1947, Bailey10 published the first results obtained with this surgical technique. Even though the recurrence rate had decreased significantly, facial nerve damage was still a risk and a possible cause of cosmetic deformities. Several changes to this technique have been published over the past 60 years, yet superficial parotidectomy is still regarded as the gold standard treatment for pleomorphic adenoma. Extracapsular dissection of superficial lobe parotid tumors was first described by Anderson15 in 1975 and
Statement of Clinical Relevance This is a systematic review of retrospective cohort studies and a meta-analysis of selected articles. The strict parameters followed to select the articles and the careful statistical analysis guarantee the accuracy of our conclusion and a high level of clinical evidence (level 2a). 663
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Table I. Selection criteria
Table II. Selection criteria for pleomorphic adenoma
Variable
Criterion
Language No. of cases Age range (y) Follow-up (mo)
English 20 18-65 12
then Gleave14 in 1979. In this approach, a very careful dissection close to the capsule was performed while preserving the nerve.8,14,15 In 1978, Iizuka and Ishikawa12 changed the technique of superficial parotidectomy and described partial superficial parotidectomy, in which the main trunk and the branches adjacent to the tumor were dissected and the tumor was removed with a 2-cm resection margin (except for the case of tumor adhesion to the nerve). The resection margin was brought to 1 cm by Witt in 2005.13 Besides facial nerve damage and recurrence of tumor, another complication of parotid surgery is the auriculotemporal nerve syndrome, widely known as Frey syndrome after the Polish neurologist who first described the exact pathogenetic mechanism. The syndrome consists of redness and sweating of the skin under auriculotemporal nerve distribution in response to gustatory stimuli. Recently, there have been significant changes to these “conservative techniques,” and many articles have been published that refer to them as minimally invasive parotidectomy. They have the advantage of fewer complications compared with the standard superficial parotidectomy; the main limitations to the use of conservative approaches are the deep lobe location of the tumor and the malignant histology. The aim of our study was to compare the conservative extracapsular parotidectomy approach and superficial parotidectomy in terms of treatment success, complication rates, and recurrence rates. A critical review of the literature and a meta-analysis were performed.
MATERIALS AND METHODS Qualitative analysis The research covered the years from 1950 to 2011, using PubMed, Ovid MEDLINE, the Cochrane Database of Systematic Reviews, and Scopus. Although extracapsular dissection was first described in 1979,14 we deemed it necessary to go back to 1950 to better understand what led surgeons to modify the surgical technique in treating pleomorphic adenoma of the parotid gland. Search keywords included pleomorphic adenoma, superficial parotidectomy, extracapsular dissection, parotid gland surgery, and benign tumor of the parotid gland. Once we had defined selection
Primary tumor Superficial lobe Size: less than 4 cm No involvement of cranial nerve VII Unifocal Unilateral Capsular integrity
criteria (Tables I and II), we screened 1152 articles including 115 reviews, and 123 articles met our inclusion criteria. While reviewing the articles, we realized that the nomenclature and classification systems of the different techniques used in parotid surgery were not the same across the authors. As Tweedie clearly pointed out in 2009,17 many centers described the same surgical procedures using different names. In Table III we have reported the nomenclatures of the procedures along with their description. We found that the Snow classification18 of 2001 was the simplest, as it groups the procedures into 5 possible surgical techniques: superficial parotidectomy, total parotidectomy, partial superficial parotidectomy, selective deep lobe parotidectomy, and extracapsular dissection. Hence we have adopted this classification in our study. Statistical analysis of 19 trials was performed. Quantitative analysis Two independent reviewers extracted the data. For each included trial, data were extracted on recurrence, permanent facial nerve paralysis, and Frey syndrome in patients who underwent extracapsular dissection or superficial parotidectomy after occurrence of primary pleomorphic adenoma; all benign tumors of parotid gland reported in the selected articles have also been included, because they represented a minority of histologic types and their contribution was deemed not able to bias the results; secondary cases and partial paralyses were conversely excluded from the analysis. Meta-analysis was conducted with the StatsDirect software, version 2.7.8 (StatsDirect Ltd). It was not possible to directly compare extracapsular dissection and superficial parotidectomy techniques, because no randomized clinical trials were found in the scientific literature. Pooled proportions with the random effect model were calculated for the incidence of permanent paralyses (defined as a permanent loss of mimic muscle function) and cases of Frey syndrome per 1000 personyears. Another pooled proportion analysis was performed on incidence rate of tumor recurrences, excluding studies with an average follow-up of less than 5 years.
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Table III. Nomenclature and surgical techniques Nomenclature superficial parotidectomy, conservative superficial parotidectomy, lateral conservative parotidectomy, classical superficial parotidectomy, complete superficial parotidectomy, lateral parotidectomy, lateral parotid lobectomy, superficial parotid lobectomy, functional superficial parotidectomy partial superficial parotidectomy, segmental parotidectomy, limited superficial parotidectomy, subtotal parotidectomy, conservative parotidectomy, partial superficial/deep lobe parotidectomy total parotidectomy, total conservative parotidectomy sparing the facial nerve radical total parotidectomy, radical parotidectomy, total parotidectomy with total facial nerve resection, total parotidectomy with partial facial nerve resection extracapsular dissection, extracapsular lumpectomy, local capsular dissection, elective local capsular dissection, partial parotidectomy intracapsular enucleation
When mean follow-up time was not available, median follow-up time was used to assess the incidence rates (as in articles by Leverstein et al.3 in 1997 and McGurk et al.23 in 2003). If neither median nor mean follow-up was available, the study was removed from the quantitative analysis (e.g., van Niekerk et al.,32 1987). Analysis of data from cases of pleomorphic adenomas and all benign tumors was conducted separately, and the respective results were reported independently.
RESULTS The results of the literature search have been summarized in Table IV. Nineteen studies were included in the quantitative analysis. Results of the data extraction are summarized in Table V. Pleomorphic adenoma recurrence pooled incidence rates were analyzed, excluding studies with a follow-up of less than 5 years. The recurrence appeared to be more common among patients with indication for superficial parotidectomy (pooled incidence rate, 2.0 cases per 1000 person-years; 95% CI, 0.9-3.6) compared with patients who underwent extracapsular dissection (1.3 cases per 1000 person-years; 95% CI, 0.4-2.9), and these results were consistent with the observations on all benign tumors (pooled incidence rate for extracapsular dissection, 0.2 cases per 1000 person-years; 95% CI, 0.1-0.8; pooled
Surgical technique Removal of superficial parotid lobe with complete nerve dissection
Selective resection of the tumor with safe margins and incomplete nerve dissection
Total parotidectomy with complete nerve dissection Total parotidectomy with facial nerve resection
Selective resection of the tumor with safe margins and complete nerve dissection
Intracapsular removal of the tumor without nerve dissection
incidence rate for superficial parotidectomy, 2.3 cases per 1000 person-years; 95% CI, 1.0-4.1), as depicted in Figures 1 and 2. Patients who underwent extracapsular dissection experienced fewer cases of total paralysis (pooled proportion, 1.1%; 95% CI, 0.3%-2.6%) compared with those who underwent superficial parotidectomy (2.2%; 95% CI, 0.4%-5.3%), as shown in Table V and Figures 3 and 4. Also, Frey syndrome was less common in patients who underwent extracapsular dissection (5.0%; 95% CI, 3.0%-7.0% vs 28%; 95% CI, 13.0%-46.0%) (see Table V and Figures 5 and 6). All these results were somewhat consistent with the outcomes observed in the all-benign-tumors population (Table V; Figures 7 to 12).
DISCUSSION Parotid surgery for pleomorphic adenomas has developed considerably in the past century, passing from minimally invasive nonradical procedure to extensive radical surgery, yet with more complications.33-36 Over the years, efforts have been aimed at finding a technique that had all the benefits of each procedure while limiting the drawbacks. Recurrences and nerve dysfunction were the main causes that prompted change in the surgical management of parotid tumors.37-41 Major advances in the surgical
Mean follow-up time (range)
Chan et al.46 (2010)
10.6 mo (0-10.5 y)
Ghosh et al.47 (2003)
12.5 y (5-20 y)
Guntinas et al.44 (2004)
74 mo (8-162 mo)
Guntinas et al.45 (2006)
3 y (1.1-12.2 y)
Hancock22 (1999)
Extracapsular dissection, 8.3 y; superficial parotidectomy, 10.3 y (3-25 y) 10.5 y (2-22 y)
Henriksson et al.48 (1998)
Laskawi et al.49 (1996)
63 mo (NA)
Leverstein et al.3 (1997)
95 mo [median] (NA)
McGurk et al.21 (1996)
12.5 y (1-34 y)
McGurk et al.23 (2003)
12 y [median] (5-30 y)
Total No. and No. of events
Extracapsular dissection (pleomorphic adenoma)
Superficial parotidectomy (pleomorphic adenoma)
N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%)
104 0 (0)
2 0 (0)
22 1 (4.5)
49 3 (6.1)
Extracapsular dissection (all benign lesions)
Superficial parotidectomy (all benign lesions)
42 0 (0)
963 56 (5.8) 59 (6.1) 46 (4.8) 120 0 (0)
491 1 (0.2) 8 (1.6) 25 (5.1)
139 5 (5.6) 2 (1.4) 45 (32.4)
171 0 (0) 0 (0) 93 (54.4)
28 0 (0) 0 (0) 0 (0)
131 0 (0) 0 (0) 9 (6.9) 380 7 (1.8) 7 (1.8) 18 (4.7)
73 0 (0) 0 (0) 18 (24.7) 181 8 (4.4)
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666
Table IV. Studies included in the quantitative analysis: data extraction
139 1 (0.7) 2 (1.4) 20 (14.0) 61 (0) (0) 8 (13.1) 95 2 (2.1) 1 (1.1) 36 (37.9)
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Author (year)
Mean follow-up time (range)
Natvig et al.50 (1994)
18 y (11-25 y)
O’Brien51 (2003)
6 y (1-14 y)
Piekarski et al.16 (2004)
34.3 mo (NA)
Prichard et al.52 (1992)
54 mo (2 y-NA)
Riad et al.53 (2011)
56.4 mo (34-93 mo)
Shehata29 (2010)
27 mo (2-72 mo)
Smith et al.8 (2007)
41 mo (5 mo-6 y)
Takahama et al.54 (2009)
56 mo (18-112 mo)
Van Niekerk et al.32 (1987)
NA (2 mo-5 y)
Extracapsular dissection (pleomorphic adenoma)
Superficial parotidectomy (pleomorphic adenoma)
N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%)
5 0 (0)
193 5 (2.6)
Extracapsular dissection (all benign lesions)
Superficial parotidectomy (all benign lesions)
355 3 (0.8) 9 (2.5) 98 8 (8.2) 8 (8.2) 31 0 (0) 0 (0) 0 (0)
15 1 (6.7) 1 (6.7) 6 (40.0)
164 5 (3.0)
26 0 (0) 0 (0) 0 (0) 12 0 (0) 0 (0) 0 (0)
11 0 (0) 0 (0) 0 (0)
368 10 (2.7) 6 (1.6) 34 (9.2) 43 1 (2.3) 5 (11.6)
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NA, not available.
Total No. and No. of events
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Table V. Results of the meta-analysis Extracapsular dissection (pleomorphic adenoma)
Superficial parotidectomy (pleomorphic adenoma)
Extracapsular dissection (all benign tumors)
Superficial parotidectomy (all benign tumors)
7 681 8 1.4 (0.7-2.5)
11* 1226* 32* * 3.0 (1.2-5.5)
5 602 1 0.3 (0-0.9)
6 1960 75 5.3 (0.9-13.4)
Total, recurrence No. of studies Total patients observed No. of cases Pooled cases per 1000 person-years (95% CI) I2 Inconsistency Total, permanent paralysis No. of studies Total patients observed No. of cases Pooled proportion, % (95% CI) I2 Inconsistency Total, Frey syndrome No. of studies Total patients observed No. of cases Pooled proportion, % (95% CI) I2 Inconsistency *One study (van Niekerk et al., available.
73*
0 4 550 7 1.1 (0.3-2.6)
7 680 16 2.2 (0.4-5.3)
21 4 550 27 5.0 (3.0-7.0)
79
95
4 560 8 1.6 (0.7-2.8) 0
5 539 175 28.0 (13.0-46.0)
13 32
0
4 560 25 3.2 (0.9-6.6) 29
94 5 1840 77 3.3 (1.4-5.9) 82 4 1485 131 18.0 (7.0-32.0) 97
1987) was excluded in the pooled analysis of the recurrence incidence because follow-up duration was not
Fig. 1. Incidence of recurrence (cases per person-year) after extracapsular dissection (pleomorphic adenoma, only studies with average follow-up 5 years).
technique have shifted the focus from recurrence rate and facial nerve damage to management of other surgical outcomes, such as Frey syndrome or hypoesthesia/ paresthesia of the earlobe as a result of the great auricular nerve damage.3,42 Examples of these advances include parotidectomy with preservation of the posterior branch of the great auricular nerve, partial superficial
parotidectomy,12,43 selective parotidectomy, and extracapsular dissection. Superficial parotidectomy is still considered the gold standard parotid gland surgery for pleomorphic adenoma. The present study focused on extracapsular dissection and its effect on recurrence rate to see whether it may represent an alternative option to superficial parotidectomy or, rather, its evolution.
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Fig. 2. Incidence of recurrence (cases per person-year) after superficial parotidectomy (pleomorphic adenoma, only studies with average follow-up 5 years).
Fig. 3. Incidence of total paralysis after extracapsular dissection (pleomorphic adenoma).
In 1993, Dallera et al.20 published the results achieved in treating 71 cases of pleomorphic adenoma by capsular dissection, with a recurrence rate of 5.4%, slightly higher than in superficial parotidectomy. In 1996, McGurk et al.21 published results on 475 cases of superficial lobe parotid pleomorphic adenomas. Extracapsular dissection was performed in 380 cases with a recurrence rate of 2% for an average follow-up of 12.5 years; these data were comparable with the rate recorded in patients undergoing superficial parotidectomy. In
1999, Hancock22 published results of a study on 42 patients treated by extracapsular dissection with an average 14-year follow-up with no reported recurrence. In 2003, McGurk et al.23 found no difference in the recurrence rate between 503 patients treated with extracapsular dissection and 159 patients undergoing superficial parotidectomy. In 2007, Smith and Komisar8 published results on 11 patients undergoing extracapsular dissection to remove pleomorphic adenoma. In a 4-month follow-up, no recurrence was reported.
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Fig. 4. Incidence of total paralysis after superficial parotidectomy (pleomorphic adenoma).
Fig. 5. Incidence of Frey syndrome after extracapsular dissection (pleomorphic adenoma).
Several factors that may influence the recurrence rate as well as nerve dysfunction have been investigated; the attention was particularly focused on capsular exposure, capsule size, capsular rupture, tumor-facial nerve interface, tumor location, tumor size, patient age, length of follow-up, and tumor histology. In 2002, Witt19 published a meta-analysis to evaluate the effect of surgical resection margins of pleomorphic adenoma on recurrences, facial nerve dysfunction, and Frey syndrome. He concluded that: - Recurrence rate in extracapsular dissection is comparable with that of superficial parotidectomy
- Transient facial nerve dysfunction rate in superficial parotidectomy is 2-fold compared with capsular dissection - The incidence of permanent facial nerve dysfunction is 1.8-fold higher in extracapsular dissection than in superficial parotidectomy - Frey syndrome is 10 times more likely to occur after superficial parotidectomy than after extracapsular dissection In the same article, the author stated that (1) for treatment of pleomorphic adenoma smaller than 4 cm, the type of surgical approach does not significantly alter
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Fig. 6. Incidence of Frey syndrome after superficial parotidectomy (pleomorphic adenoma).
Fig. 7. Incidence rate of recurrence in cases per person-year (95% CI) after extracapsular dissection (all benign tumors).
the major complications (capsular exposure, capsular rupture, recurrence, permanent facial nerve dysfunction); (2) the amount of parotid tissue resected is directly proportional to the rate of transient nerve dysfunction and Frey syndrome; (3) capsular exposure frequently occurs in small parotid pleomorphic adenomas (less than 4 cm) regardless of the amount of parotid tissue removed; (4) in tumors strongly adherent to the nerve, minimally invasive techniques (such as extracapsular dissection) do not allow complete removal, owing to interruptions in the capsule and
pseudopodia, and thus they are not recommended; (5) capsular rupture leads to increased recurrence rate irrespective of the amount of parotid tissue sacrifice; (6) the surgeon’s experience plays a major role in recurrence rate reduction; and (7) the recurrence rate remains high in intracapsular enucleation.19 Over the past decades histopathologic features and clinical behavior of pleomorphic adenoma have been investigated.6,26-39 This tumor is characterized by cell pleomorphism, which includes epithelial and myoepithelial elements mixed with stromal cells that may be
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Fig. 8. Incidence rate of recurrence in cases per person-year (95% CI) after superficial parotidectomy (all benign tumors).
Fig. 9. Incidence of total paralysis after extracapsular dissection (all benign tumors).
myxoid, mucoid, or chondroid enclosed in an incomplete capsule (pseudocapsule).3-28 The technique of choice for surgical management of pleomorphic adenoma has to take into account those histopathologic features, because incomplete excision or breach of the tumor’s pseudocapsule are the only proved causes for increased recurrence rate.30-33 In 2007, Zbaren and Stauffer25 published findings from a histopathologic study on 218 cases of pleomorphic adenoma. The purpose of the study was to evaluate the relationship between histologic features
(incomplete capsule, capsular infiltration, pseudopodia, and satellite nodules), tumor size, and histology. The study found a close relationship between capsular interruption and stromal subtype but no relationship with tumor size; tumor capsular penetration and pseudopodia were mostly present in the conventional or cellular rather than stromal subtype, but again no correlation with tumor size was found; conversely, the study pointed out that the larger the tumor the more likely the presence of satellite nodules.
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Fig. 10. Incidence of total paralysis after superficial parotidectomy (all benign tumors).
Fig. 11. Incidence of Frey syndrome after extracapsular dissection (all benign tumors).
Histologic findings showed that tumor removal with margins of healthy tissue is arduous to achieve in sizable tumors, and in those adherent to the nerve. Even in the case of superficial parotidectomy, dissection adjacent to the capsule involves many parts of the tumor.17 Hence, tumor removal with healthy margins of tissue can be performed only when the mass is small and embedded in the central portion of the superficial lobe. Indeed, in 60% of cases the tumor margins are close to the facial nerve and dissection adherent to the
capsule is, therefore, mandatory.29 Yet, interestingly, even though on histologic examination excision is incomplete, the recurrence rate after superficial parotidectomy is low compared with cases of tumor enucleation.17 The results of our meta-analysis showed that extracapsular dissection may represent a viable alternative option to superficial parotidectomy in the treatment of pleomorphic adenoma, for the following reasons:
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Fig. 12. Incidence of Frey syndrome after superficial parotidectomy (all benign tumors).
- The recurrence rate is higher in the group of patients treated with superficial parotidectomy - Superficial parotidectomy has a higher incidence of facial nerve paralysis and Frey syndrome than extracapsular dissection No randomized clinical trials on extracapsular dissection and superficial parotidectomy were found in our literature review, which made it impossible to directly compare the results of the 2 techniques. Furthermore, the selection of surgical approach was often based on the surgeon’s preference rather than on the tumor characteristics. In examining the articles selected for our metaanalysis, we realized that some studies involved small samples,8,23 which might have biased outcomes; in other cases, the same patients were enrolled in subsequent trials.21-23,44,45 Follow-up significantly differed for patients enrolled in the same trial and among different studies; indeed, in some of them follow-up was based on telephone interviews. All recurrences, however, were always diagnosed by physicians. In some studies,16,29,46 the average follow-up was too short to provide reliable evaluation of the recurrence rate, but the estimate of actual recurrence rate after removal of pleomorphic adenomas may be deemed optimistic.
CONCLUSIONS Based on our literature review and ensuing meta-analysis, we may conclude that in patients with unilateral pleomorphic adenoma, located in the superficial lobe, sized less than 4 cm and with no clinical involvement of
cranial nerve VII, extracapsular dissection represents a viable alternative option to superficial parotidectomy in terms of successful outcome, convenience, and ease of performance. These findings are consistent with results obtained from the evaluation of all benign tumors. On the other hand, extracapsular dissection should not be considered in cases involving sizable tumors with poor mobility (4 cm), malignant histology, or parotid deep lobe involvement. REFERENCES 1. Ellis GL, Auclair PL. Atlas of Tumor Pathology: Tumors of the Salivary Glands. Washington, DC: Armed Forces Institute of Pathology; 1996. 2. Seifert G, Sobin LH. World Health Organization Classification of Tumours: Histopathological Classification of Tumors. Berlin, Germany: Springer-Verlag; 1991. 3. Leverstein H, Van Der Wal JE, Tiwari RM, Van Der Waal I, Snow GB. Surgical management of 246 previously untreated pleomorphic adenomas of the parotid gland. Br J Surg. 1997;84:399-403. 4. Batsakis JG. Tumors of the major salivary glands. In: Tumors of the Head and Neck: Clinical and Pathological Considerations. 2nd ed. Baltimore, MD: Williams and Wilkins; 1979:1-76. 5. McEvedy PG. Diseases of the salivary glands. Clin J. 1934;63: 334-338. 6. Rawsom AJ, Howard JM, Royster HI, Horn RC Jr. Tumors of the salivary glands: a clinicopathological study of 160 cases. Cancer. 1950;3:445-458. 7. Senn N. The pathology and surgical treatment of tumors. Philadelphia, PA: W.B. Saunders; 1895. 8. Smith S, Komisar A. Limited parotidectomy: the role of extracapsular dissection in parotid gland neoplasms. Laryngoscope. 2007;117:1163-1167. 9. Janes RM. The treatment of tumors of the salivary gland by radical excision. Can Med Assoc J. 1940;43:554-559. 10. Bailey H. Parotidectomy: indications and results. BMJ. 1947;1: 404-407.
OOOO Volume 117, Number 6 11. Patey DH, Thackray AC. The treatment of parotid tumours in the light of a pathological study of a parotidectomy material. Br J Surg. 1957;45:477-487. 12. Iizuka K, Ishikawa K. Surgical techniques for benign parotid tumors: segmental resection vs extracapsular lumpectomy. Acta Otolaryngol. 1998;537(suppl):75-81. 13. Witt RL. Minimally invasive surgery for parotid pleomorphic adenoma. Ear Nose Throat J. 2005;84:308-311. 14. Gleave EN, Whittaker JS, Nicholson A. Salivary tumoursd experience over thirty years. Clin Otolaryngol Allied Sci. 1979;4: 247-257. 15. Anderson R. Benign mixed tumours of the parotid gland. In: Chambers RG, Janssen de Limpens AMP, Jaques DA, Routledge RT, eds. Cancer of the Head and Neck: Proceedings of an International Symposium, Montreux, Switzerland, April 2-4, 1975. International Congress Series, No. 365. Amsterdam, The Netherlands: Excerpta Medica; 1975:1555-1558. 16. Piekarski J, Nejc D, Szymczak W, Wronski K, Jeziorski A. Results of extracapsular dissection of pleomorphic adenoma of parotid gland. J Oral Maxillofac Surg. 2004;62:11981202. 17. Tweedie DJ. Surgery of the parotid gland: evolution of techniques, nomenclature and a precise classification system. Clin Otolaryngol. 2009;34:303-308. 18. Snow GB. The surgical approaches to the treatment of parotid pleomorphic adenomas. In: McGurk M, Renehan AG, eds. Controversies in the Management of Salivary Gland Disease. Oxford, England: Oxford University Press; 2001:chap 5, 58. 19. Witt R. The significance of the margin in parotid surgery for pleomorphic adenoma. Laryngoscope. 2002;112:2141-2154. 20. Dallera P, Marchetti C, Campobassi A. Local capsular dissection of parotid pleomorphic adenomas. Int J Oral Maxillofac Surg. 1993;22:154-157. 21. McGurk M, Renehan A, Gleave EN, Hancock BD. Clinical significance of the tumor capsule in the treatment of parotid adenomas. Br J Surg. 1996;83:1747-1749. 22. Hancock BD. Clinically benign parotid tumours: local dissection as an alternative to superficial parotidectomy in selected cases. Ann R Coll Surg Engl. 1999;81:299-301. 23. McGurk M, Thoams BL, Reneham AG. Extracapsular dissection for clinically benign parotid lumps: reduced morbidity without oncological compromise. Br J Cancer. 2003;89:1610-1613. 24. Donovan DT, Conley JJ. Capsular significance in parotid tumor surgery: reality and myths of lateral lobectomy. Laryngoscope. 1984;94:324-329. 25. Zbaren P, Stauffer E. Pleomorphic adenoma of the parotid gland: histopathologic analysis of the capsular characteristics of 218 tumors. Head Neck. 2007;29:751-757. 26. Paris J, Facon F, Chrestian MA, Giovanni A, Zanaret M. Pleomorphic adenoma of the parotid: histopathologic study. Ann Otolaryngol Chir Cervicofac. 2004;121:161-166. 27. Stennert E, Guntinas-Lichius O, Klussmann JP, Arnold G. Histopathology of pleomorphic adenoma in the parotid gland: a prospective unselected series of 100 cases. Laryngoscope. 2001;111:2195-2200. 28. Seifert G, Brocheriou C, Cardessa A, Eveson JW. WHO international histological classification of tumours: tentative histological classification of salivary gland tumours. Pathol Res Pract. 1990;186:555-581. 29. Shehata EA. Extracapsular dissection for benign parotid tumours. Int J Oral Maxillofac Surg. 2010;39:140-144. 30. Stennert ES, Wittekindt C, Klussmann JP, Arnold G, GuntinasLichius O. Recurrent pleomorphic adenoma of the parotid gland: a prospective histopathological and immunohistochemical study. Laryngoscope. 2004;114:158-163.
REVIEW ARTICLE Foresta et al. 675 31. McFarland J. Three hundred mixed tumors of the salivary glands of which 69 recurred. Surg Clin North Am. 1921;1:1515-1521. 32. Van Niekerk JL, Wobbes TH, Monstrey S, Bruaset I. The management of parotid tumors: a ten-year experience. Acta Chir Belg. 1987;87:1-5. 33. Spiro RH. Salivary neoplasms: overview of a 35-year experience with 2,807 patients. Head Neck Surg. 1986;8:177-184. 34. Hugo NE, McKinney P, Griffith BH. Management of tumors of the parotid gland. Surg Clin North Am. 1973;53:105-111. 35. Haw CS. Pleomorphic adenoma of the parotid gland: a review of results of treatment. J R Coll Surg Edinb. 1975;20:25-29. 36. Conley J, Clairmont AA. Facial nerve in recurrent benign pleomorphic adenoma. Arch Otolaryngol. 1979;105:247-251. 37. Renehan A, Gleave EN, McGurk M. An analysis of the treatment of 114 patients with recurrent pleomorphic adenomas of the parotid gland. Am J Surg. 1996;172:710-714. 38. Stanley RE, Mackenzie IJ, Maran AG. The surgical approach to recurrent pleomorphic adenoma of the parotid gland. Ann Acad Med Singapore. 1984;13:91-95. 39. Patel N, Poole A. Recurrent benign parotid tumours: the lesson not learnt yet? Aust N Z J Surg. 1998;68:562-564. 40. Maran AG, Mackenzie IJ, Stanley RE. Recurrent pleomorphic adenomas of the parotid gland. Arch Otolaryngol. 1984;110: 167-171. 41. Carew JF, Spiro RH, Singh B, Shah JP. Treatment of recurrent pleomorphic adenomas of the parotid gland. Otolaryngol Head Neck Surg. 1999;5:539-542. 42. Laccourreye H, Laccourreye O, Cauchois R, Jouffre V, Ménard M, Brasnu D. Total conservative parotidectomy for primary benign pleomorphic adenoma of the parotid gland: a 25-year experience with 229 patients. Laryngoscope. 1994;104:1487-1494. 43. Rea JL. Partial parotidectomies: morbidity and benign tumor recurrence rates in a series of 94 cases. Laryngoscope. 2000;110: 924-927. 44. Guntinas-Lichius O, Kick C, Klussmann JP, Jungehuelsing M, Stennert E. Pleomorphic adenoma of the parotid gland: a 13year experience of consequent management by lateral or total parotidectomy. Eur Arch Otorhinolaryngol. 2004;261: 143-146. 45. Guntinas-Lichius O, Klussmann JP, Wittekindt C, Stennert E. Parotidectomy for benign parotid disease at a university teaching hospital: outcome of 963 operations. Laryngoscope. 2006;116: 534-540. 46. Chan WH, Lee KW, Chiang FY, Ho KY, Chai CY, Kuo WR. Features of parotid gland disease and surgical results in southern Taiwan. Kaohsiung J Med Sci. 2010;26:483-492. 47. Ghosh S, Panarese A, Bull PD, Lee JA. Marginally excised parotid pleomorphic salivary adenomas: risk factors for recurrence and management. A 12.5-year mean follow-up study of histologically marginal excisions. Clin Otolaryngol. 2003;28: 262-266. 48. Henriksson G, Westrin KM, Carlsöö B, Silfverswärd C. Recurrent primary pleomorphic adenomas of salivary gland origin: intrasurgical rupture, histopathologic features, and pseudopodia. Cancer. 1998;82:617-620. 49. Laskawi R, Schott T, Mirzaie-Petri M, Schroeder M. Surgical management of pleomorphic adenomas of the parotid gland: a follow-up study of three methods. J Oral Maxillofac Surg. 1996;54:1176-1179. 50. Natvig K, Søberg R. Relationship of intraoperative rupture of pleomorphic adenomas to recurrence: an 11-25 year follow-up study. Head Neck. 1994;16:213-217. 51. O’Brien CJ. Current management of benign parotid tumors: the role of limited superficial parotidectomy. Head Neck. 2003;25: 946-952.
ORAL AND MAXILLOFACIAL SURGERY 676 Foresta et al. 52. Prichard AJ, Barton RP, Narula AA. Complications of superficial parotidectomy versus extracapsular lumpectomy in the treatment of benign parotid lesions. J R Coll Surg Edinb. 1992;37:155-158. 53. Riad MA, Abdel-Rahman H, Ezzat WF, Adly A, Dessouky O, Shehata M. Variables related to recurrence of pleomorphic adenomas: outcome of parotid surgery in 182 cases. Laryngoscope. 2011;121:1467-1472. 54. Takahama Junior A, Almeida OP, Kowalski LP. Parotid neoplasms: analysis of 600 patients attended at a single institution. Braz J Otorhinolaryngol. 2009;75:497-501.
OOOO June 2014 Reprint requests: Andrea Torroni, MD, PhD Maxillo-Facial Surgery Department Complesso Integrato Columbus Catholic University Medical School Via Giuseppe Moscati 31 00168 Rome Italy [email protected]
Pleomorphic adenoma and benign parotid tumors: extracapsular dissection vs superficial parotidectomydreview of literature and meta-analysis Enrico Foresta, MD,a Andrea Torroni, MD, PhD,a Francesco Di Nardo, MD,b Chiara de Waure, MD,b Andrea Poscia, MD,b Giulio Gasparini, MD,a Tito Matteo Marianetti, MD,a and Sandro Pelo, MDa Complesso Integrato Columbus, Catholic University Medical School, Rome, Italy; Institute of Nuclear Medicine, Catholic University of the Sacred Heart, Rome, Italy
Objective. This study compared extracapsular dissection (ED) vs superficial parotidectomy (SP) in the treatment of pleomorphic adenoma and benign parotid tumors. Study Design. The research covered the years 1950-2011 in PubMed, Ovid MEDLINE, the Cochrane Database of Systematic Reviews, and Scopus. Of 1152 articles screened, 123 studies met the inclusion criteria. A review of the nomenclature of the different parotid surgery techniques was done. Recurrence rate, permanent facial nerve paralysis, and Frey syndrome of patients who underwent ED vs those who underwent SP were compared by meta-analysis. Results. Our meta-analysis data comparing ED and SP found that: (1) the recurrence rate is higher in patients treated with SP; (2) SP has a higher incidence of cranial nerve VII paralysis; and (3) Frey syndrome is more common after SP. Conclusions. ED may be a viable option in the treatment of unilateral benign parotid tumors of the superficial lobe, sized less than 4 cm, without involvement of the facial nerve. (Oral Surg Oral Med Oral Pathol Oral Radiol 2014;117:663-676)
Tumors of the salivary glands represent 3% to 10% of all head and neck neoplasms1-15; 75% to 85% of them originate in the parotid gland, and 70% to 80% are benign. Most involve the superficial lobe of the parotid, which accounts for 80% of the gland parenchyma.8,16-29 The most common benign tumors of the parotid gland are pleomorphic adenoma and Warthin tumor. Pleomorphic adenomas lack a complete capsule and are surrounded by healthy gland tissue, which is compressed as they grow. They often present with very small outgrowths extending to the adjacent tissue. It is commonly believed that this histologic feature accounts for their clinical behavior, multicentricity, and recurrence over time.1-3,11,14,21,24-30 The close relationship between the gland and the facial nerve, as well as the high recurrence rate, has shaped surgical techniques for parotid gland neoplasms over the years.17 Enucleation was first described by Senn7 in 1895 as the surgical technique of choice. It was not accompanied by facial nerve dissection. Removal of the tumor was incomplete, as there was tissue left behind. This procedure was widely used in parotid gland tumors for 30 years. In 1921, Sistrunk modified this technique, adding retrograde dissection of a
Maxillo-Facial Surgery, Complesso Integrato Columbus, Catholic University Medical School. b Institute of Nuclear Medicine, Catholic University of the Sacred Heart. Received for publication Jun 7, 2013; returned for revision Feb 11, 2014; accepted for publication Feb 18, 2014. Ó 2014 Elsevier Inc. All rights reserved. 2212-4403/$ - see front matter http://dx.doi.org/10.1016/j.oooo.2014.02.026
the mandibular branch of the facial nerve.8 The treatment of parotid pleomorphic adenoma remained substantially unsuccessful until 1940, owing to a high recurrence rate (45%) and facial nerve paralysis,3,5,6,31 prompting more in-depth microscopic studies of pleomorphic adenomas and modifications of surgical techniques. In 1940, Janes9 published his first article on salivary gland tumor surgery by parotidectomy with dissection and preservation of the main trunk and branches of the facial nerve. In this procedure, the whole superficial lobe was removed along with the tumor. In 1947, Bailey10 published the first results obtained with this surgical technique. Even though the recurrence rate had decreased significantly, facial nerve damage was still a risk and a possible cause of cosmetic deformities. Several changes to this technique have been published over the past 60 years, yet superficial parotidectomy is still regarded as the gold standard treatment for pleomorphic adenoma. Extracapsular dissection of superficial lobe parotid tumors was first described by Anderson15 in 1975 and
Statement of Clinical Relevance This is a systematic review of retrospective cohort studies and a meta-analysis of selected articles. The strict parameters followed to select the articles and the careful statistical analysis guarantee the accuracy of our conclusion and a high level of clinical evidence (level 2a). 663
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Table I. Selection criteria
Table II. Selection criteria for pleomorphic adenoma
Variable
Criterion
Language No. of cases Age range (y) Follow-up (mo)
English 20 18-65 12
then Gleave14 in 1979. In this approach, a very careful dissection close to the capsule was performed while preserving the nerve.8,14,15 In 1978, Iizuka and Ishikawa12 changed the technique of superficial parotidectomy and described partial superficial parotidectomy, in which the main trunk and the branches adjacent to the tumor were dissected and the tumor was removed with a 2-cm resection margin (except for the case of tumor adhesion to the nerve). The resection margin was brought to 1 cm by Witt in 2005.13 Besides facial nerve damage and recurrence of tumor, another complication of parotid surgery is the auriculotemporal nerve syndrome, widely known as Frey syndrome after the Polish neurologist who first described the exact pathogenetic mechanism. The syndrome consists of redness and sweating of the skin under auriculotemporal nerve distribution in response to gustatory stimuli. Recently, there have been significant changes to these “conservative techniques,” and many articles have been published that refer to them as minimally invasive parotidectomy. They have the advantage of fewer complications compared with the standard superficial parotidectomy; the main limitations to the use of conservative approaches are the deep lobe location of the tumor and the malignant histology. The aim of our study was to compare the conservative extracapsular parotidectomy approach and superficial parotidectomy in terms of treatment success, complication rates, and recurrence rates. A critical review of the literature and a meta-analysis were performed.
MATERIALS AND METHODS Qualitative analysis The research covered the years from 1950 to 2011, using PubMed, Ovid MEDLINE, the Cochrane Database of Systematic Reviews, and Scopus. Although extracapsular dissection was first described in 1979,14 we deemed it necessary to go back to 1950 to better understand what led surgeons to modify the surgical technique in treating pleomorphic adenoma of the parotid gland. Search keywords included pleomorphic adenoma, superficial parotidectomy, extracapsular dissection, parotid gland surgery, and benign tumor of the parotid gland. Once we had defined selection
Primary tumor Superficial lobe Size: less than 4 cm No involvement of cranial nerve VII Unifocal Unilateral Capsular integrity
criteria (Tables I and II), we screened 1152 articles including 115 reviews, and 123 articles met our inclusion criteria. While reviewing the articles, we realized that the nomenclature and classification systems of the different techniques used in parotid surgery were not the same across the authors. As Tweedie clearly pointed out in 2009,17 many centers described the same surgical procedures using different names. In Table III we have reported the nomenclatures of the procedures along with their description. We found that the Snow classification18 of 2001 was the simplest, as it groups the procedures into 5 possible surgical techniques: superficial parotidectomy, total parotidectomy, partial superficial parotidectomy, selective deep lobe parotidectomy, and extracapsular dissection. Hence we have adopted this classification in our study. Statistical analysis of 19 trials was performed. Quantitative analysis Two independent reviewers extracted the data. For each included trial, data were extracted on recurrence, permanent facial nerve paralysis, and Frey syndrome in patients who underwent extracapsular dissection or superficial parotidectomy after occurrence of primary pleomorphic adenoma; all benign tumors of parotid gland reported in the selected articles have also been included, because they represented a minority of histologic types and their contribution was deemed not able to bias the results; secondary cases and partial paralyses were conversely excluded from the analysis. Meta-analysis was conducted with the StatsDirect software, version 2.7.8 (StatsDirect Ltd). It was not possible to directly compare extracapsular dissection and superficial parotidectomy techniques, because no randomized clinical trials were found in the scientific literature. Pooled proportions with the random effect model were calculated for the incidence of permanent paralyses (defined as a permanent loss of mimic muscle function) and cases of Frey syndrome per 1000 personyears. Another pooled proportion analysis was performed on incidence rate of tumor recurrences, excluding studies with an average follow-up of less than 5 years.
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Table III. Nomenclature and surgical techniques Nomenclature superficial parotidectomy, conservative superficial parotidectomy, lateral conservative parotidectomy, classical superficial parotidectomy, complete superficial parotidectomy, lateral parotidectomy, lateral parotid lobectomy, superficial parotid lobectomy, functional superficial parotidectomy partial superficial parotidectomy, segmental parotidectomy, limited superficial parotidectomy, subtotal parotidectomy, conservative parotidectomy, partial superficial/deep lobe parotidectomy total parotidectomy, total conservative parotidectomy sparing the facial nerve radical total parotidectomy, radical parotidectomy, total parotidectomy with total facial nerve resection, total parotidectomy with partial facial nerve resection extracapsular dissection, extracapsular lumpectomy, local capsular dissection, elective local capsular dissection, partial parotidectomy intracapsular enucleation
When mean follow-up time was not available, median follow-up time was used to assess the incidence rates (as in articles by Leverstein et al.3 in 1997 and McGurk et al.23 in 2003). If neither median nor mean follow-up was available, the study was removed from the quantitative analysis (e.g., van Niekerk et al.,32 1987). Analysis of data from cases of pleomorphic adenomas and all benign tumors was conducted separately, and the respective results were reported independently.
RESULTS The results of the literature search have been summarized in Table IV. Nineteen studies were included in the quantitative analysis. Results of the data extraction are summarized in Table V. Pleomorphic adenoma recurrence pooled incidence rates were analyzed, excluding studies with a follow-up of less than 5 years. The recurrence appeared to be more common among patients with indication for superficial parotidectomy (pooled incidence rate, 2.0 cases per 1000 person-years; 95% CI, 0.9-3.6) compared with patients who underwent extracapsular dissection (1.3 cases per 1000 person-years; 95% CI, 0.4-2.9), and these results were consistent with the observations on all benign tumors (pooled incidence rate for extracapsular dissection, 0.2 cases per 1000 person-years; 95% CI, 0.1-0.8; pooled
Surgical technique Removal of superficial parotid lobe with complete nerve dissection
Selective resection of the tumor with safe margins and incomplete nerve dissection
Total parotidectomy with complete nerve dissection Total parotidectomy with facial nerve resection
Selective resection of the tumor with safe margins and complete nerve dissection
Intracapsular removal of the tumor without nerve dissection
incidence rate for superficial parotidectomy, 2.3 cases per 1000 person-years; 95% CI, 1.0-4.1), as depicted in Figures 1 and 2. Patients who underwent extracapsular dissection experienced fewer cases of total paralysis (pooled proportion, 1.1%; 95% CI, 0.3%-2.6%) compared with those who underwent superficial parotidectomy (2.2%; 95% CI, 0.4%-5.3%), as shown in Table V and Figures 3 and 4. Also, Frey syndrome was less common in patients who underwent extracapsular dissection (5.0%; 95% CI, 3.0%-7.0% vs 28%; 95% CI, 13.0%-46.0%) (see Table V and Figures 5 and 6). All these results were somewhat consistent with the outcomes observed in the all-benign-tumors population (Table V; Figures 7 to 12).
DISCUSSION Parotid surgery for pleomorphic adenomas has developed considerably in the past century, passing from minimally invasive nonradical procedure to extensive radical surgery, yet with more complications.33-36 Over the years, efforts have been aimed at finding a technique that had all the benefits of each procedure while limiting the drawbacks. Recurrences and nerve dysfunction were the main causes that prompted change in the surgical management of parotid tumors.37-41 Major advances in the surgical
Mean follow-up time (range)
Chan et al.46 (2010)
10.6 mo (0-10.5 y)
Ghosh et al.47 (2003)
12.5 y (5-20 y)
Guntinas et al.44 (2004)
74 mo (8-162 mo)
Guntinas et al.45 (2006)
3 y (1.1-12.2 y)
Hancock22 (1999)
Extracapsular dissection, 8.3 y; superficial parotidectomy, 10.3 y (3-25 y) 10.5 y (2-22 y)
Henriksson et al.48 (1998)
Laskawi et al.49 (1996)
63 mo (NA)
Leverstein et al.3 (1997)
95 mo [median] (NA)
McGurk et al.21 (1996)
12.5 y (1-34 y)
McGurk et al.23 (2003)
12 y [median] (5-30 y)
Total No. and No. of events
Extracapsular dissection (pleomorphic adenoma)
Superficial parotidectomy (pleomorphic adenoma)
N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%)
104 0 (0)
2 0 (0)
22 1 (4.5)
49 3 (6.1)
Extracapsular dissection (all benign lesions)
Superficial parotidectomy (all benign lesions)
42 0 (0)
963 56 (5.8) 59 (6.1) 46 (4.8) 120 0 (0)
491 1 (0.2) 8 (1.6) 25 (5.1)
139 5 (5.6) 2 (1.4) 45 (32.4)
171 0 (0) 0 (0) 93 (54.4)
28 0 (0) 0 (0) 0 (0)
131 0 (0) 0 (0) 9 (6.9) 380 7 (1.8) 7 (1.8) 18 (4.7)
73 0 (0) 0 (0) 18 (24.7) 181 8 (4.4)
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Author (year)
666
Table IV. Studies included in the quantitative analysis: data extraction
139 1 (0.7) 2 (1.4) 20 (14.0) 61 (0) (0) 8 (13.1) 95 2 (2.1) 1 (1.1) 36 (37.9)
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Author (year)
Mean follow-up time (range)
Natvig et al.50 (1994)
18 y (11-25 y)
O’Brien51 (2003)
6 y (1-14 y)
Piekarski et al.16 (2004)
34.3 mo (NA)
Prichard et al.52 (1992)
54 mo (2 y-NA)
Riad et al.53 (2011)
56.4 mo (34-93 mo)
Shehata29 (2010)
27 mo (2-72 mo)
Smith et al.8 (2007)
41 mo (5 mo-6 y)
Takahama et al.54 (2009)
56 mo (18-112 mo)
Van Niekerk et al.32 (1987)
NA (2 mo-5 y)
Extracapsular dissection (pleomorphic adenoma)
Superficial parotidectomy (pleomorphic adenoma)
N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%) N Recurrence (%) Paralysis (%) Frey syndrome (%)
5 0 (0)
193 5 (2.6)
Extracapsular dissection (all benign lesions)
Superficial parotidectomy (all benign lesions)
355 3 (0.8) 9 (2.5) 98 8 (8.2) 8 (8.2) 31 0 (0) 0 (0) 0 (0)
15 1 (6.7) 1 (6.7) 6 (40.0)
164 5 (3.0)
26 0 (0) 0 (0) 0 (0) 12 0 (0) 0 (0) 0 (0)
11 0 (0) 0 (0) 0 (0)
368 10 (2.7) 6 (1.6) 34 (9.2) 43 1 (2.3) 5 (11.6)
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NA, not available.
Total No. and No. of events
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Table IV. Continued
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Table V. Results of the meta-analysis Extracapsular dissection (pleomorphic adenoma)
Superficial parotidectomy (pleomorphic adenoma)
Extracapsular dissection (all benign tumors)
Superficial parotidectomy (all benign tumors)
7 681 8 1.4 (0.7-2.5)
11* 1226* 32* * 3.0 (1.2-5.5)
5 602 1 0.3 (0-0.9)
6 1960 75 5.3 (0.9-13.4)
Total, recurrence No. of studies Total patients observed No. of cases Pooled cases per 1000 person-years (95% CI) I2 Inconsistency Total, permanent paralysis No. of studies Total patients observed No. of cases Pooled proportion, % (95% CI) I2 Inconsistency Total, Frey syndrome No. of studies Total patients observed No. of cases Pooled proportion, % (95% CI) I2 Inconsistency *One study (van Niekerk et al., available.
73*
0 4 550 7 1.1 (0.3-2.6)
7 680 16 2.2 (0.4-5.3)
21 4 550 27 5.0 (3.0-7.0)
79
95
4 560 8 1.6 (0.7-2.8) 0
5 539 175 28.0 (13.0-46.0)
13 32
0
4 560 25 3.2 (0.9-6.6) 29
94 5 1840 77 3.3 (1.4-5.9) 82 4 1485 131 18.0 (7.0-32.0) 97
1987) was excluded in the pooled analysis of the recurrence incidence because follow-up duration was not
Fig. 1. Incidence of recurrence (cases per person-year) after extracapsular dissection (pleomorphic adenoma, only studies with average follow-up 5 years).
technique have shifted the focus from recurrence rate and facial nerve damage to management of other surgical outcomes, such as Frey syndrome or hypoesthesia/ paresthesia of the earlobe as a result of the great auricular nerve damage.3,42 Examples of these advances include parotidectomy with preservation of the posterior branch of the great auricular nerve, partial superficial
parotidectomy,12,43 selective parotidectomy, and extracapsular dissection. Superficial parotidectomy is still considered the gold standard parotid gland surgery for pleomorphic adenoma. The present study focused on extracapsular dissection and its effect on recurrence rate to see whether it may represent an alternative option to superficial parotidectomy or, rather, its evolution.
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Fig. 2. Incidence of recurrence (cases per person-year) after superficial parotidectomy (pleomorphic adenoma, only studies with average follow-up 5 years).
Fig. 3. Incidence of total paralysis after extracapsular dissection (pleomorphic adenoma).
In 1993, Dallera et al.20 published the results achieved in treating 71 cases of pleomorphic adenoma by capsular dissection, with a recurrence rate of 5.4%, slightly higher than in superficial parotidectomy. In 1996, McGurk et al.21 published results on 475 cases of superficial lobe parotid pleomorphic adenomas. Extracapsular dissection was performed in 380 cases with a recurrence rate of 2% for an average follow-up of 12.5 years; these data were comparable with the rate recorded in patients undergoing superficial parotidectomy. In
1999, Hancock22 published results of a study on 42 patients treated by extracapsular dissection with an average 14-year follow-up with no reported recurrence. In 2003, McGurk et al.23 found no difference in the recurrence rate between 503 patients treated with extracapsular dissection and 159 patients undergoing superficial parotidectomy. In 2007, Smith and Komisar8 published results on 11 patients undergoing extracapsular dissection to remove pleomorphic adenoma. In a 4-month follow-up, no recurrence was reported.
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Fig. 4. Incidence of total paralysis after superficial parotidectomy (pleomorphic adenoma).
Fig. 5. Incidence of Frey syndrome after extracapsular dissection (pleomorphic adenoma).
Several factors that may influence the recurrence rate as well as nerve dysfunction have been investigated; the attention was particularly focused on capsular exposure, capsule size, capsular rupture, tumor-facial nerve interface, tumor location, tumor size, patient age, length of follow-up, and tumor histology. In 2002, Witt19 published a meta-analysis to evaluate the effect of surgical resection margins of pleomorphic adenoma on recurrences, facial nerve dysfunction, and Frey syndrome. He concluded that: - Recurrence rate in extracapsular dissection is comparable with that of superficial parotidectomy
- Transient facial nerve dysfunction rate in superficial parotidectomy is 2-fold compared with capsular dissection - The incidence of permanent facial nerve dysfunction is 1.8-fold higher in extracapsular dissection than in superficial parotidectomy - Frey syndrome is 10 times more likely to occur after superficial parotidectomy than after extracapsular dissection In the same article, the author stated that (1) for treatment of pleomorphic adenoma smaller than 4 cm, the type of surgical approach does not significantly alter
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Fig. 6. Incidence of Frey syndrome after superficial parotidectomy (pleomorphic adenoma).
Fig. 7. Incidence rate of recurrence in cases per person-year (95% CI) after extracapsular dissection (all benign tumors).
the major complications (capsular exposure, capsular rupture, recurrence, permanent facial nerve dysfunction); (2) the amount of parotid tissue resected is directly proportional to the rate of transient nerve dysfunction and Frey syndrome; (3) capsular exposure frequently occurs in small parotid pleomorphic adenomas (less than 4 cm) regardless of the amount of parotid tissue removed; (4) in tumors strongly adherent to the nerve, minimally invasive techniques (such as extracapsular dissection) do not allow complete removal, owing to interruptions in the capsule and
pseudopodia, and thus they are not recommended; (5) capsular rupture leads to increased recurrence rate irrespective of the amount of parotid tissue sacrifice; (6) the surgeon’s experience plays a major role in recurrence rate reduction; and (7) the recurrence rate remains high in intracapsular enucleation.19 Over the past decades histopathologic features and clinical behavior of pleomorphic adenoma have been investigated.6,26-39 This tumor is characterized by cell pleomorphism, which includes epithelial and myoepithelial elements mixed with stromal cells that may be
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Fig. 8. Incidence rate of recurrence in cases per person-year (95% CI) after superficial parotidectomy (all benign tumors).
Fig. 9. Incidence of total paralysis after extracapsular dissection (all benign tumors).
myxoid, mucoid, or chondroid enclosed in an incomplete capsule (pseudocapsule).3-28 The technique of choice for surgical management of pleomorphic adenoma has to take into account those histopathologic features, because incomplete excision or breach of the tumor’s pseudocapsule are the only proved causes for increased recurrence rate.30-33 In 2007, Zbaren and Stauffer25 published findings from a histopathologic study on 218 cases of pleomorphic adenoma. The purpose of the study was to evaluate the relationship between histologic features
(incomplete capsule, capsular infiltration, pseudopodia, and satellite nodules), tumor size, and histology. The study found a close relationship between capsular interruption and stromal subtype but no relationship with tumor size; tumor capsular penetration and pseudopodia were mostly present in the conventional or cellular rather than stromal subtype, but again no correlation with tumor size was found; conversely, the study pointed out that the larger the tumor the more likely the presence of satellite nodules.
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Fig. 10. Incidence of total paralysis after superficial parotidectomy (all benign tumors).
Fig. 11. Incidence of Frey syndrome after extracapsular dissection (all benign tumors).
Histologic findings showed that tumor removal with margins of healthy tissue is arduous to achieve in sizable tumors, and in those adherent to the nerve. Even in the case of superficial parotidectomy, dissection adjacent to the capsule involves many parts of the tumor.17 Hence, tumor removal with healthy margins of tissue can be performed only when the mass is small and embedded in the central portion of the superficial lobe. Indeed, in 60% of cases the tumor margins are close to the facial nerve and dissection adherent to the
capsule is, therefore, mandatory.29 Yet, interestingly, even though on histologic examination excision is incomplete, the recurrence rate after superficial parotidectomy is low compared with cases of tumor enucleation.17 The results of our meta-analysis showed that extracapsular dissection may represent a viable alternative option to superficial parotidectomy in the treatment of pleomorphic adenoma, for the following reasons:
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Fig. 12. Incidence of Frey syndrome after superficial parotidectomy (all benign tumors).
- The recurrence rate is higher in the group of patients treated with superficial parotidectomy - Superficial parotidectomy has a higher incidence of facial nerve paralysis and Frey syndrome than extracapsular dissection No randomized clinical trials on extracapsular dissection and superficial parotidectomy were found in our literature review, which made it impossible to directly compare the results of the 2 techniques. Furthermore, the selection of surgical approach was often based on the surgeon’s preference rather than on the tumor characteristics. In examining the articles selected for our metaanalysis, we realized that some studies involved small samples,8,23 which might have biased outcomes; in other cases, the same patients were enrolled in subsequent trials.21-23,44,45 Follow-up significantly differed for patients enrolled in the same trial and among different studies; indeed, in some of them follow-up was based on telephone interviews. All recurrences, however, were always diagnosed by physicians. In some studies,16,29,46 the average follow-up was too short to provide reliable evaluation of the recurrence rate, but the estimate of actual recurrence rate after removal of pleomorphic adenomas may be deemed optimistic.
CONCLUSIONS Based on our literature review and ensuing meta-analysis, we may conclude that in patients with unilateral pleomorphic adenoma, located in the superficial lobe, sized less than 4 cm and with no clinical involvement of
cranial nerve VII, extracapsular dissection represents a viable alternative option to superficial parotidectomy in terms of successful outcome, convenience, and ease of performance. These findings are consistent with results obtained from the evaluation of all benign tumors. On the other hand, extracapsular dissection should not be considered in cases involving sizable tumors with poor mobility (4 cm), malignant histology, or parotid deep lobe involvement. REFERENCES 1. Ellis GL, Auclair PL. Atlas of Tumor Pathology: Tumors of the Salivary Glands. Washington, DC: Armed Forces Institute of Pathology; 1996. 2. Seifert G, Sobin LH. World Health Organization Classification of Tumours: Histopathological Classification of Tumors. Berlin, Germany: Springer-Verlag; 1991. 3. Leverstein H, Van Der Wal JE, Tiwari RM, Van Der Waal I, Snow GB. Surgical management of 246 previously untreated pleomorphic adenomas of the parotid gland. Br J Surg. 1997;84:399-403. 4. Batsakis JG. Tumors of the major salivary glands. In: Tumors of the Head and Neck: Clinical and Pathological Considerations. 2nd ed. Baltimore, MD: Williams and Wilkins; 1979:1-76. 5. McEvedy PG. Diseases of the salivary glands. Clin J. 1934;63: 334-338. 6. Rawsom AJ, Howard JM, Royster HI, Horn RC Jr. Tumors of the salivary glands: a clinicopathological study of 160 cases. Cancer. 1950;3:445-458. 7. Senn N. The pathology and surgical treatment of tumors. Philadelphia, PA: W.B. Saunders; 1895. 8. Smith S, Komisar A. Limited parotidectomy: the role of extracapsular dissection in parotid gland neoplasms. Laryngoscope. 2007;117:1163-1167. 9. Janes RM. The treatment of tumors of the salivary gland by radical excision. Can Med Assoc J. 1940;43:554-559. 10. Bailey H. Parotidectomy: indications and results. BMJ. 1947;1: 404-407.
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OOOO June 2014 Reprint requests: Andrea Torroni, MD, PhD Maxillo-Facial Surgery Department Complesso Integrato Columbus Catholic University Medical School Via Giuseppe Moscati 31 00168 Rome Italy [email protected]
