Lesões do nervo facial relacionadas à parotidectomia: proposta de um sistema Sunnybrook de graduação facial modificado

Arq Neuropsiquiatr anp Arquivos de Neuro-Psiquiatria Arq. Neuro-Psiquiatr. 0004-282X 1678-4227 Academia Brasileira de Neurologia - ABNEURO RESUMO A lesão do nervo facial é a principal complicação neurológica relacionada às parotidectomias e, em geral, o ramo marginal mandibular é o mais frequentemente acometido. Objetivo Testar um Sistema Sunnybrook de Graduação Facial modificado (mS-FGS) como uma nova ferramenta para avaliar a função do nervo facial após a parotidectomia, enfatizando o ramo marginal mandibular. Métodos Estudo retrospectivo, baseado em prontuários de 73 casos (40 do sexo feminino, 18-84 anos, idade média = 53,2), submetidos à parotidectomia, com preservação do nervo facial. Todos os pacientes apresentavam neoplasias parotídeas ou câncer de pele avançado, e foram tratados pela autora principal entre 2006 e 2014. Resultados Neste estudo, os músculos inervados pelo ramo marginal mandibular foram os mais acometidos (72,6% dos casos), principalmente nos pacientes que realizaram esvaziamento cervical (p = 0,023). Os Escores de Movimento Voluntário obtidos pelo sistema modificado foram inferiores aos obtidos pelo original (p < 0,001). As melhores pontuações foram observadas em pacientes com tumores benignos parotídeos e os piores resultados, naqueles com câncer de pele. Pacientes que necessitaram de esvaziamento cervical e ressecção de outras estruturas, além da parótida, apresentaram escores menores (p = 0,031 e p = 0,021), evidenciados apenas pelo sistema modificado. Os tumores malignos geraram escores significativamente menores, independentemente do instrumento empregado. A análise pós fisioterapia envolveu 50 casos. Os piores resultados, após a intervenção fisioterapêutica, também foram observados nos músculos inervados pelo ramo marginal mandibular. Conclusão A avaliação da disfunção facial pós-parotidectomia, através do Sistema Sunnybrook com a modificação proposta permitiu uma apreciação mais detalhada do ramo marginal mandibular, sem prejuízo à avaliação dos demais ramos. Parotidectomy, the main treatment for benign or malignant parotid tumors, is also indicated in advanced skin tumors invading the gland or spreading to the parotid lymph nodes1. Surgery involves facial nerve manipulation at its trunk and branches. Although facial nerve preservation is aimed, especially in patients without previous weakness2, the incidence of immediate post-parotidectomy facial nerve dysfunction is high, reaching 14.5% of permanent deficits3. Causes may be related to the surgery, or the underlying disease4,5. The marginal mandibular branch (MMB) is the most frequently affected3,5,6,7, resulting in an inability to show the lower teeth on the affected side due to weakness of the depressor labii inferioris (DLI) and depressor anguli oris (DAO) muscles8. The Sunnybrook Facial Grading System (S-FGS) was recently recommended as the standard tool for assessing facial nerve dysfunctions9. However, the muscles innervated by the MMB are not considered by this instrument. The objective was to emphasize the importance of the MMB dysfunction as a frequent complication following parotidectomy and propose a modified S-FGS that significantly improves the overall clinical assessment of the facial nerve. METHODS This was a retrospective study involving post-parotidectomy patients with dysfunctional facial nerves, treated at the Physiotherapy Department, National Cancer Institute, Rio de Janeiro, Brazil, between January 2006 and December 2014. During this period, a qualified and experienced physiotherapist (MGSTC) personally followed the study patients. Patients had been referred to the physiotherapy outpatient clinic by surgeons or physiotherapists responsible for inpatient care. At the first outpatient physiotherapy appointment (median time after surgery: 28 days, interquartile range [IQR]: 21–37), the assessment of the five standard facial expressions (forehead wrinkle, eye closure, smile, snarl and lip pucker) was performed as recommended by the S-FGS. Additionally, the DLI and DAO integrity was evaluated using the same criteria through the command “show the lower teeth”. In edentulous patients, the command was adapted to “turn down the lower lip”. According to the S-FGS, each expression receives a degree ranging from 1 to 5, where 1 means no movement, and 5 means full movement, compared with the normal side. The voluntary movement (VM) score is calculated by adding the individual degrees of movement of the five expressions and multiplying the result by 4. This result forms a composite score with two other components, resting symmetry and synkinesis. For the VM scores, patients with total facial paralysis receive 20 points, and those with normal facial movements get 100 points. The proposed modified Sunnybrook system (mS-FGS) consisted of removing the “snarl” expression, performed by the levator labii superioris and levator labii superioris alaeque nasi muscles (one of the three expressions performed by muscles predominantly innervated by the buccal branch); and inserting the “show the lower teeth” expression, performed by the DLI and DAO muscles, innervated by the MMB. We then calculated the VM score using both the original and mS-FGS versions. After facial movement assessments, patients with mild dysfunctions and spontaneous recovery were released. The remaining patients started an individualized physiotherapy program, including self-massage and facial mirror exercises, according to treatment-based categories10,11. Stretching, for healthy hemiface muscles, was prescribed when necessary. Every patient received a manual containing instructions for home exercises to be performed three times a day, with mirror biofeedback, until complete recovery. In the subsequent appointments, patients with low degrees of facial movement received additional Proprioceptive Neuromuscular Facilitation and stimulation with ice12,13. Patients were periodically reassessed, following the same protocol. The mean number of physical therapy appointments was 5.40 (2–11), and the median interval time between the first and last facial evaluations was 133 days (IQR: 53–269). The final analysis involved 50 patients. The Mann-Whitney and Kruskal-Wallis nonparametric tests were used to contrast the degree of movement in the DLI/DAO and the VM scores (original and modified) with the categorical variables. The Wilcoxon test was used to analyze the difference between original and modified VM scores, and the score variation between the initial and final times. The analyses were performed using an SPSS software version 17. A 95% confidence interval was considered significant. The research project was approved by the National Cancer Institute Research Ethics Committee under registration number 49889015.0.0000.5274, in October 2015. RESULTS From the initial 175 post-parotidectomy patients, 67 were excluded in the first evaluation, as 10 had received physiotherapy treatment only during hospitalization, and 57 had facial nerve sacrifice at the level of the trunk or branches. Among the remaining 108 patients, 36 were excluded for various reasons (Table 1). The final sample comprised 72 patients originating from 73 cases (one patient was operated on twice): 40 women (54.8%), with a mean age of 53.2 years (18–84 years). By the last evaluation, we had lost patients because of the following reasons: they had been released from physical therapy due to spontaneous recovery (10 patients), abandonment of treatment (eight patients), no proper records of a second evaluation (four patients) and death (one patient). Table 1 Patient exclusions. Reason n (%) Physiotherapy for another disorder (pain, trismus, etc.) 10 (27.0) Patient treated by another physiotherapist* 7 (18.9) Lack of voluntary movement evaluation records 7 (18.9) Resection of facial expressions muscles 5 (13.5) Cognitive deficit 3 (8.1) Younger than 18 years 2 (5.4) Previous facial nerve dysfunction 1 (2.7) Incomplete medical records 1 (2.7) Total 36 (100) *examined just once by the researcher. Parotidectomy was performed because of benign and malignant parotid neoplasms or advanced skin cancer. Clinical and surgical data are depicted in Table 2. About one third of the patients (30.1%) needed resection of other structures beyond the parotid, mostly the preauricular skin. Enlarged procedures included the auricular pavilion (partial or entire), auditory canal, sternocleidomastoid muscle, among others. Reconstruction, required in 23 patients, was performed using techniques selected according to the defect dimension – advancement, unilobed, bilobed, pectoralis major and deltopectoral flaps, among others. In five benign disease patients, the reconstruction with fat graft was used for prevention of Frey’s syndrome. Only one patient had undergone previous radiotherapy. Pleomorphic adenoma was the most frequent benign parotid disease (68.4%). Regarding malignant tumors, mucoepidermoid carcinoma was the major parotid neoplasm (33.3%), whereas squamous cell carcinoma and melanoma accounted for 65% of skin cancers. Table 2 Clinical surgical characteristics of the sample (total and subgroups). Variables Median (Q1; Q3) or N (%) Total Benign parotid Malignant parotid Skin cancer Participants 73 (100) 38 (52.0) 15 (20.6) 20 (27.4) Age, years 57 (38; 68) 48 (38; 63) 43 (27; 70) 67 (58; 75) ≥60 years old 31 (52.5) 13 (34.2) 4 (26.7) 6 (30) Female sex 40 (54.8) 26 (68.4) 8 (53.3) 6 (30) Race White 41 (56.2) 17 (44.7) 6 (40.0) 18 (90) Black 12 (16.4) 8 (21.1) 4 (26.7) 0 Brown 19 (26) 12 (31.6) 5 (33.3) 2 (10) Tumor side Right 41 (56.2) 23 (60.5) 7 (46.7) 11 (55) Left 31 (42.5) 14 (36.8) 8 (53.3) 9 (45) Bilateral 1 (1.4) 1 (2.6) 0 0 Evolution time, months 16 (10; 36) 24 (11; 60) 24 (8; 36) 12 (5; 24) Type of parotidectomy Superficial 62 (84.9) 33 (86.8) 10 (66.7) 19 (95) Total 11 (15.1) 5 (13.2) 5 (33.3) 1 (5) Resection of other structures* 22 (30.1) 0 4 (26.8) 18 (90) Submandibular gland inclusion 5 (6.8) 0 1 (6.7) 4 (20) Neck dissection 22 (30.1) 0 7 (46.7) 15 (75) Dissection of level I 7 (9.6) 0 2 (13.3) 5 (25) Previous parotid surgery 7 (9.6) 5 (13.2) 2 (13.3) 0 Reconstruction 23 (31.5) 5 (13.2) 4 (26.7) 14 (70) Adjuvant radiotherapy 14 (19.2) 0 7 (46.7) 7 (35) *beyond the gland. FRO: Frontalis; OO: Orbicularis oculi; ZYG/RIS: Zygomaticus/Risorius; LLA/LLS: Levator labii superioris alaeque nasi/Levator labii superioris; OOS/OOI: Orbicularis oris (superior and inferior); DLI/DAO: Depressor labii inferioris and depressor anguli oris. Figure 1 shows the distribution of degrees of movement from each evaluated expression. The most affected muscles were the ones innervated by the MMB (DLI/DAO), where the lowest degrees of movement (1–3) were observed in 72.6% of the patients. Almost 40% of these patients received a score of 1 degree (no movement). The second most affected muscle was the orbicularis oris (49.3%). In some patients, the inferior portion of this muscle is also innervated by the MMB. Figure 1 Distribution of degree of movement in facial expressions – first evaluation. Note a high percentage of patients with the lower degrees in DLI/DAO muscles, an examination that is not included in the original S-FGS. The DLI/DAO movements did not vary according to clinical variables (age, primary site, malignancy). Patients submitted for neck dissection, either in the total sample (p = 0.023) or in the malignant parotid subgroup (p = 0.054), had statistically significant lower degrees of movement. Patients who required resection of level I lymph nodes (seven patients) and submandibular gland (five patients), both located at the submandibular triangle, also had low DLI/DAO degrees of movement. However, this difference did not reach statistical significance. The five patients who underwent reconstruction with fat graft had higher DLI/DAO degrees of movement (p = 0.004). The same was observed in patients with malignant parotid disease, re-operated upon because of tumor recurrence (p = 0.038). These findings were unexpected, especially the latter, since the risk of facial nerve damage in re-operations is higher. As re-operations occurred in only two patients, this finding was attributed to chance (Table 3). Table 3 Surgical variables and analysis of degrees of movement of the DLI/DAO. Variables Mean (SD) or p-value Total Benign parotid Malignant parotid Skin cancer DLI/DAO p-value DLI/DAO p-value DLI/DAO p-value DLI/DAO p-value Parotidectomy Superficial 2.6 (1.5) 0.403 2.8 (1.5) 0.376 2.2 (1.4) 0.859 ** ** Total 2.2 (1.6) 2.2 (1.8) 2.4 (1.7) Neck dissection No 2.8 (1.6) 0.023 * * 2.9 (1.5) 0.054 2.6 (2.2) 0.866 Yes 1.9 (1.4) 1.6 (1.1) 2.1 (1.5) Dissection of level I No 2.2 (1.6) 0.332 * * 2.4 (1.5) 0.571 2.5 (1.8) 0.197 Yes 1.3 (0.5) 1.5 (0.7) 1.2 (0.4) Submandibular gland inclusion No 2.0 (1.5) 0.967 * * ** ** 2.4 (1.7) 0.335 Yes 1.5 (0.6) 1.3 (0.5) Resection of other structures No 2.7 (1.6) 0.060 * * 2.6 (1.6) 0.343 3.0 (2.8) 0.674 Yes 2.0 (1.4) 1.5 (0.6) 2.1 (1.6) Reconstruction No 2.5 (1.5) 0.848 2.5 (1.4) 0.004 2.5 (1.6) 0.571 2.8 (2.0) 0.547 Yes 2.5 (1.6) 4.6 (0.5) 1.8 (0.9) 1.9 (1.4) Parotid gland reoperation No 2.5 (1.6) 0.891 2.9 (1.5) 0.084 1.9 (1.2) 0.038 * * Yes 2.4 (1.6) 1.6 (0.9) 4.5 (0.7) DLI/DAO: depressor labii inferioris and depressor anguli oris movement grades; Values in bold were statistically significant; * Not performed; ** Not tested. Just one patient underwent some of the procedures. The VM scores (five facial expressions assessment) were higher when calculated by the original system (median = 80 points, IQR: 54–100). Patients with benign diseases had higher median scores (92 points) than those with malignant parotid tumors (68 points) and skin cancer (64 points), but this difference was not significant (p = 0.071). The VM scores obtained with the mS-FGS were significantly lower in both the total sample and subgroups. Using the mS-FGS, the VM scores were different among subgroups (p = 0.036). The 12 patients who underwent more complex surgeries (parotidectomy, resection of other structures, neck dissection and reconstruction) had the lowest median score (50 points; IQR: 41–83). In contrast, the 38 patients with benign disease had the best results (median = 82; IQR: 63–92). Full movement (100 points) was assigned to 20 patients (27.4%) using the original system, contrasting with only 7 (9.7%) using the mS-FGS (Table 4). Table 4 Differences between voluntary movement scores assessed by the original and the modified systems – First evaluation. Variables Total Benign parotid Malignant parotid Skin Cancer n = 73 n = 38 n = 15 n = 20 Original Score Average (SD) 74.19 (26.35) 81.47 (21.59) 65.87 (29.28) 66.6 (29.02) Median (IQR) 80 (54 - 100) 92 (67 - 100) 68 (28 - 92) 64 (44 - 99) Highest score (100 pts) - n (%) 20 (27.4) 13 (34.2) 2 (13.3) 5 (25.0) Lowest scores (20-36 pts) - n (%) 10 (13.7) 2 (5.3) 4 (26.7) 4 (20.0) Modified Score Average (SD) 69.70 (23.89) 77.05 (19.61) 61.60 (26.69) 61.8 (25.77) Median (IQR) 76 (52 - 92) 82 (63 - 92) 68 (32 - 80) 60 (41 - 84) Highest score (100 pts) - n (%) 7 (9.6) 4 (10.5) 2 (13.3) 1 (5.0) Lowest scores (20-36 pts) - n (%) 10 (13.7) 2 (5.3) 4 (26.7) 4 (20.0) Mean difference between scores (min-max) - 4.49 (-16 to 8) - 4.42 (-16 to 8) - 4.26 (-16 to 8) - 4.80 (-16 to 8) Difference between scores (p-value) < 0.001 < 0.001 0.031 0.018 pts: points. Voluntary movement score values (original and modified) were significantly lower in patients with malignant disease, regardless of the instrument used (p = 0.022 and p = 0.010, respectively). Patients who required neck dissection or resection of other structures beyond the parotid gland had also lower scores, which were only observed with the mS-FGS (Table 5). Table 5 Analysis of original and modified voluntary movement scores in relation to clinical-surgical variables. Variable Original VM Score Modified VM Score Mean (SD) p-value Mean (SD) p-value Malignant Yes 66.3 (29.0) 0.022 61.7 (25.8) 0.010 No 81.5 (21.6) 77.1 (19.6) Disease Benign parotid 81.5 (21.6) 0.071 77.1 (19.6) 0.036 Malignant parotid 65.9 (29.9) 61.6 (26.7) Skin cancer 66.6 (29.0) 61.8 (25.8) Parotidectomy Superficial 76.2 (25.6) 0.101 71.6 (23.0) 0.169 Total 62.9 (29,2) 59.3 (27.5) Neck dissection Yes 66.9 (27.8) 0.121 60.9 (24.0) 0.031 No 77.3 (25.3) 73.5 (23.1) Resection of other structures Yes 64.4 (29.2) 0.065 59.5 (25.5) 0.021 No 78.4 (24.1) 74.1 (22.0) Submandibular gland inclusion Yes 57.6 (32.2) 0.251 52.8 (27.6) 0.138 No 75.5 (25.6) 70.9 (23.4) Reconstruction Yes 70.4 (29.0) 0.556 65.9 (27.0) 0.512 No 75.9 (25.1) 71.4 (22.4) Parotid gland reoperation Yes 68.6 (25.3) 0.448 65.1 (25.1) 0.554 No 74.8 (26.6) 70.2 (23.9) Values in bold were statistically significant. FRO: Frontalis; OO: Orbicularis oculi; ZYG/RIS: Zygomaticus/Risorius; LLA/LLS: Levator labii superioris alaeque nasi/Levator labii superioris; OOS/OOI: Orbicularis oris (superior and inferior); DLI/DAO: Depressor labii inferioris and depressor anguli oris. In the last evaluation, the outcomes from the 50 remaining patients showed significant improvement in VM scores, regardless of the disease and the system used. However, the worst outcomes were observed in muscles innervated by the MMB, with 17 patients (34%) maintaining the lowest degree of movement (Figure 2). The isolated MMB paresis was observed in 10 patients, eight of them with benign diseases. Figure 2 Distribution of degrees of movement in facial expressions – last evaluation. DISCUSSION The facial nerve provides innervation for facial expression muscles, and asymmetry is immediately evident and upsetting following facial nerve lesions14. This study showed that a modified version of the S-FGS—the mS-FGS, including evaluation of the DLI and DAO muscles—significantly improved the overall assessment of facial nerve dysfunctions following parotidectomy. Several other instruments are available to clinically assess facial nerve impairments9,15,16. The most popular is the House-Brackmann Facial Nerve Grading System (HB), which grades the facial nerve function in six levels17. This system has received criticism due to the propensity for interobserver variation and low sensitivity to facial changes over the time18. Moreover, the HB has limitations in accurately distinguishing different degrees of dysfunction among the facial nerve branches19-21. This distinction is indispensable for the physical therapist to plan the best treatment, compare results and predict the functional prognosis. Even the Facial Nerve Grading Scale 2.0 (the revised HB)22, which proposes a regional evaluation of the face, does not enable the evaluator to distinguish whether the dysfunction of the oral region is related to the buccal branch, or to the MMB, or both. An adapted HB approach has been used to assess the facial nerve branches post-parotidectomy23. However, some aspects of this method were not clear, such as the criteria to objectively differentiate between some discrete nuances of the HB grades (III and IV), and which muscles or facial expressions were selected to assess each branch (especially the buccal). New instruments have been created, focusing on a more reliable evaluation with greater reproducibility. The S-FGS stands out in this sense24. It offers a regional assessment, considering the face at rest and during movements, beyond the synkinesis, and with good intraobserver and interobserver reliability.9 The five standard expressions cover the temporal, zygomatic and buccal branches. However, muscles predominantly innervated by the MMB are not included in the system, limiting the test’s use for post-parotidectomy assessment (Figure 3). Other instruments include the evaluation of lip depression, such as the Sydney19, and Yanagihara25 facial nerve grading systems, but the S-FGS surpasses them, mainly in relation to the details of other components (resting symmetry and synkinesis). Figure 3 Patient on the 35th postoperative day of superficial parotidectomy due to a left benign parotid disease. Using only the original S-FGS, the isolated MMB dysfunction would not be adequately documented. Authorized image. The Post-Parotidecomy Facial Nerve Grading System was specifically developed for this purpose26, but its applicability and efficiency have not yet been tested by other authors. On the other hand, Fattah et al.9, on behalf of the Sir Charles Bell Society, “…recommend widespread adoption of the Sunnybrook Facial Grading Scale as the current standard in reporting outcomes of facial nerve disorders”, based on their systematic review of 19 facial nerve grading scales.9 This excellent tool, however, needs adaptation to better appraise parotidectomy-induced facial dysfunction by including the MMB evaluation. Otherwise, these muscles need to be assessed apart, hindering a consolidated result that would reliably reflect the post-operative facial functional status. Our attempt to add the new expression to the S-FGS, without removing any item failed, as the composite score is based on weights. The inclusion of the sixth expression would hinder the maintenance of the individual values and the weights that compose the instrument, completely mischaracterizing it. In contrast, by withdrawing the snarl expression, we counterbalanced the new inclusion. This occurred because the buccal branch, which innervates the muscles of the snarl expression, maintains its integrity tested by two other important expressions: smiling (zygomaticus and risorius muscles) and lip pucker (orbicularis oris muscle). With the new method, the appraisal of the temporal and zygomatic branches, performed by the frontalis and orbicularis oculi muscles, remains unchanged. Since the cervical branch innervates only the platysma muscle, it was not considered here or in the original system. Although the present study emphasized the VM scores, owing to the proposal of the inclusion of the MMB, we reinforced the importance of other S-FGS components, such as resting symmetry, which was not changed. Considering the synkinesis grading, the expressions involved with the more frequent manifestations of aberrant reinnervation (forehead wrinkle, close eyes, and smile) were mantained27. The question arises as why the MMB is the most affected facial nerve branch in parotidectomies. Nichols et al.28 argued that the reason was related to the fact that the MMB was thinner and longer than nerves that originated from the upper division. The relationship between the extent of facial nerve dissection and subsequent facial paresis was studied by Cannon et al3. The longest branch was the MMB (145mm), and, among their 11 patients with transient facial paresis, 10 involved this branch. Another possible reason was the lower number of vertical interconnections evidenced in the inferior branches compared with those in the upper branches29,30. In our study, the MMB was also the most affected, especially in patients with malignant parotid tumors who underwent neck dissection, which imposed an increased risk to the MMB due to the nerve manipulation distal to the parotid gland. This risk is higher during dissection of level I, located in submandibular triangle, although injuries may also occur at the top of level II31-33. Guntinas-Lichius et al.21 described that among their 79 patients with malignant parotid tumors submitted to total parotidectomy with facial nerve sparing, 76% required neck dissection. Forty patients (51%) presented with MMB dysfunction as evidenced by electromyography21. The increased risk to the MMB, by the inclusion of the level IB in the neck dissection of patients undergoing parotidectomy, was also emphasized by Møller et al33. In our sample, patients who required level I dissection presented with a considerable weakness of the MMB muscles, although this did not reach statistical significance. The high DLI/DAO movement scores in patients who underwent reconstruction with fat graft for prevention of Frey’s syndrome caught our attention. We did not find reports supporting this finding. Speculatively, we believe that these surgeries presented a low technical difficulty if the tumors were small (1.5–3.0 cm), benign (pleomorphic adenomas) and encapsulated, and were completely excised. The mean VM score of these patients was also high (above 92 points, regardless of the S-FGS version used), suggesting low morbidity of the procedure to the facial nerve as a whole. Concerning the global facial assessment, we found significantly lower VM scores using the mS-FGS, and a statistically significant difference among the subgroup scores was observed. This difference was expected because enlarged surgeries tend to result in more severe facial nerve damage. Malignant tumors, neck dissection and resection of other structures were associated with lower VM scores, but the last two findings were identified only by the mS-FGS. Worse results in malignant tumors have been justified by more aggressive surgical requirements34. Higher incidences of facial weakness were noted in patients with malignant parotid tumors arising from the deep lobe (100%) and in those requiring neck dissection (83%)35. Neck dissection was also associated with 3.5-times higher odds of facial palsy36. Concerning the resection of other structures, several parotidectomy reports related to skin cancer have addressed the diagnosis, treatment, and prognosis of the disease, but only reported the percentage of sacrifice or preservation of the nerve37,38,39. A series comprising 22 operations for cutaneous tumors including intra- and extraparotid nerve dissection showed that “… the rate of transient facial nerve dysfunction after cutaneous surgery for skin tumors is slightly higher than after superficial or partial parotidectomy for benign parotid gland tumors40. We had 13 patients with isolated MMB paresis, most of them secondary to benign diseases that would not have been measured objectively if we had used only the original S-FGS. Patients with isolated MMB paresis (17%), evidenced by electromyography, were reported in a study of 963 parotidectomies for benign diseases41. Tung et al.5 reported that all patients who developed immediate facial weakness after parotidectomy presented with MMB impairment. The percentage of isolated MMB paresis among these patients reached 93%5. The MMB, besides being the most frequently affected, tends to be responsible for most of the permanent dysfunctions35,41,42. Likewise, our results revealed a worse MMB recovery in comparison with the other branches. Seventeen patients (34%) maintained the lower DLI/DAO degrees of movement, of whom 6 (35%) had a benign disease, 8 (47%) had skin cancer and 7 (41%) underwent neck dissection. Taken together, the data reinforce the importance of the MMB in the follow-up of parotidectomy patients. Our study has some limitations. Although the time frame of this retrospective evaluation spanned eight years, the number of patients in each subgroup was small, probably due to the restrictive inclusion and exclusion criteria. There was no inter-rater evaluation or electromyographic examination. Nevertheless, our results robustly suggest that post-parotidectomy facial nerve dysfunction is not adequately documented using the unmodified S-FGS. The inclusion of a detailed evaluation of the MMB, the most-frequently affected by surgery, makes the system more suitable for the post-parotidectomy assessments. The proposed modification, replacing the snarl expression by showing the lower teeth, enables the evaluation of this branch without hindering the appraisal of the other branches. The adoption of a standardized instrument, that is able to accurately reflect the global facial function, as well as the different impairments that are possible in each branch, favors a superior rehabilitation follow-up. A prospective study with a larger sample size may confirm the present findings. In conclusion, the standard facial nerve evaluation tool, the S-FGS, fails to accurately capture dysfunction of the MMB. A modified S-FGS consisting of replacing the “snarl” expression by the “showing the lower teeth” improves the global assessment of the facial nerve involving MMB lesions. References 1 1. Gandolfi MM, Slattery W 3rd. Parotid gland tumors and the facial nerve. Otolaryngol Clin North Am. 2016 Apr;49(2):425-34. https://doi.org/10.1016/j.otc.2015.12.001 Gandolfi MM Slattery W 3rd Parotid gland tumors and the facial nerve Otolaryngol Clin North Am 2016 04 49 2 425 434 https://doi.org/10.1016/j.otc.2015.12.001 2 2. Guntinas-Lichius O. The facial nerve in the presence of a head and neck neoplasm: assessment and outcome after surgical management. Curr Opin Otolaryngol Head Neck Surg. 2004 Apr;12(2):133-41. https://doi.org/10.1097/00020840-200404000-00014 Guntinas-Lichius O The facial nerve in the presence of a head and neck neoplasm: assessment and outcome after surgical management Curr Opin Otolaryngol Head Neck Surg 2004 04 12 2 133 141 https://doi.org/10.1097/00020840-200404000-00014 3 3. Cannon CR, Replogle WH, Schenk MP. Facial nerve in parotidectomy: a topographical analysis. Laryngoscope. 2004 Nov;114(11):2034-7. https://doi.org/10.1097/01.mlg.0000147943.13052.62 Cannon CR Replogle WH Schenk MP Facial nerve in parotidectomy: a topographical analysis Laryngoscope 2004 11 114 11 2034 2037 https://doi.org/10.1097/01.mlg.0000147943.13052.62 4 4. Dulguerov P, Marchal F, Lehmann W. Postparotidectomy facial nerve paralysis: possible etiologic factors and results with routine facial nerve monitoring. Laryngoscope. 1999 May;109(5):754-62. https://doi.org/10.1097/00005537-199905000-00014 Dulguerov P Marchal F Lehmann W Postparotidectomy facial nerve paralysis: possible etiologic factors and results with routine facial nerve monitoring Laryngoscope 1999 05 109 5 754 762 https://doi.org/10.1097/00005537-199905000-00014 5 5. Tung BK, Chu PY, Tai SK, Wang YF, Tsai TL, Lee TL, et al. Predictors and timing of recovery in patients with immediate facial nerve dysfunction after parotidectomy. Head Neck. 2014 Feb;36(2):247-51. https://doi.org/10.1002/hed.23287 Tung BK Chu PY Tai SK Wang YF Tsai TL Lee TL et al Predictors and timing of recovery in patients with immediate facial nerve dysfunction after parotidectomy Head Neck 2014 02 36 2 247 251 https://doi.org/10.1002/hed.23287 6 6. Gaillard C, Périé S, Susini B, St Guily JL. Facial nerve dysfunction after parotidectomy: the role of local factors. Laryngoscope. 2005 Feb;115(2):287-91. https://doi.org/10.1097/01.mlg.0000154735.61775.cd Gaillard C Périé S Susini B St Guily JL Facial nerve dysfunction after parotidectomy: the role of local factors Laryngoscope 2005 02 115 2 287 291 https://doi.org/10.1097/01.mlg.0000154735.61775.cd 7 7. Musani MA, Zafar A, Suhail Z, Malik S, Mirza D. Facial nerve morbidity following surgery for benign parotid tumours. J Coll Physicians Surg Pak. 2014 Aug;24(8):569-72. Musani MA Zafar A Suhail Z Malik S Mirza D Facial nerve morbidity following surgery for benign parotid tumours J Coll Physicians Surg Pak 2014 08 24 8 569 572 8 8. Baker DC, Conley J. Avoiding facial nerve injuries in rhytidectomy. Anatomical variations and pitfalls. Plast Reconstr Surg. 1979 Dec;64(6):781-95. https://doi.org/10.1097/00006534-197912000-00005 Baker DC Conley J Avoiding facial nerve injuries in rhytidectomy. Anatomical variations and pitfalls Plast Reconstr Surg 1979 12 64 6 781 795 https://doi.org/10.1097/00006534-197912000-00005 9 9. Fattah AY, Gurusinghe AD, Gavilan J, Hadlock TA, Marcus JR, Marres H, et al. Sir Charles Bell Society. Facial nerve grading instruments: systematic review of the literature and suggestion for uniformity. Plast Reconstr Surg. 2015 Feb;135(2):569-79. https://doi.org/10.1097/PRS.0000000000000905 Fattah AY Gurusinghe AD Gavilan J Hadlock TA Marcus JR Marres H et al Sir Charles Bell Society Facial nerve grading instruments: systematic review of the literature and suggestion for uniformity Plast Reconstr Surg 2015 02 135 2 569 579 https://doi.org/10.1097/PRS.0000000000000905 10 10. Brach JS, VanSwearingen JM. Physical therapy for facial paralysis: a tailored treatment approach. Phys Ther. 1999 Apr;79(4):397-404. Brach JS VanSwearingen JM Physical therapy for facial paralysis: a tailored treatment approach Phys Ther 1999 04 79 4 397 404 11 11. Vanswearingen J. Facial rehabilitation: a neuromuscular reeducation, patient-centered approach. Facial Plast Surg. 2008 May;24(2):250-9. https://doi.org/10.1055/s-2008-1075841 Vanswearingen J Facial rehabilitation: a neuromuscular reeducation, patient-centered approach Facial Plast Surg 2008 05 24 2 250 259 https://doi.org/10.1055/s-2008-1075841 12 12. Barbara M, Antonini G, Vestri A, Volpini L, Monini S. Role of Kabat physical rehabilitation in Bell’s palsy: a randomized trial. Acta Otolaryngol. 2010;130(1):167-72. https://doi.org/10.3109/00016480902882469 Barbara M Antonini G Vestri A Volpini L Monini S Role of Kabat physical rehabilitation in Bell’s palsy: a randomized trial Acta Otolaryngol 2010 130 1 167 172 https://doi.org/10.3109/00016480902882469 13 13. Adler SS, Beckers D, Buck M. PNF - Facilitação neuromuscular proprioceptiva. 2nd ed. São Paulo: Manole; 2007. Adler SS Beckers D Buck M PNF - Facilitação neuromuscular proprioceptiva 2nd São Paulo Manole 2007 14 14. Gilchrist JM. Seventh cranial neuropathy. Semin Neurol. 2009 Feb;29(1):5-13. https://doi.org/10.1055/s-0028-1124018 Gilchrist JM Seventh cranial neuropathy Semin Neurol 2009 02 29 1 5 13 https://doi.org/10.1055/s-0028-1124018 15 15. Chee GH, Nedzelski JM. Facial nerve grading systems. Facial Plast Surg. 2000;16(4):315-24. https://doi.org/10.1055/s-2000-15547 Chee GH Nedzelski JM Facial nerve grading systems Facial Plast Surg. 2000 16 4 315 324 https://doi.org/10.1055/s-2000-15547 16 16. Kang TS, Vrabec JT, Giddings N, Terris DJ. Facial nerve grading systems (1985-2002): beyond the House-Brackmann scale. Otol Neurotol. 2002 Sep;23(5):767-71. https://doi.org/10.1097/00129492-200209000-00026 Kang TS Vrabec JT Giddings N Terris DJ Facial nerve grading systems (1985-2002): beyond the House-Brackmann scale Otol Neurotol 2002 09 23 5 767 771 https://doi.org/10.1097/00129492-200209000-00026 17 17. House JW, Brackmann DE. Facial nerve grading system. Otolaryngol Head Neck Surg. 1985 Apr;93(2):146-7. https://doi.org/10.1177/019459988509300202 House JW Brackmann DE Facial nerve grading system Otolaryngol Head Neck Surg 1985 04 93 2 146 147 https://doi.org/10.1177/019459988509300202 18 18. Kanerva M, Poussa T, Pitkäranta A. Sunnybrook and House-Brackmann Facial Grading systems: intrarater repeatability and interrater agreement. Otolaryngol Head Neck Surg. 2006 Dec;135(6):865-71. https://doi.org/10.1016/j.otohns.2006.05.748 Kanerva M Poussa T Pitkäranta A Sunnybrook and House-Brackmann Facial Grading systems: intrarater repeatability and interrater agreement Otolaryngol Head Neck Surg 2006 12 135 6 865 871 https://doi.org/10.1016/j.otohns.2006.05.748 19 19. Coulson SE, Croxson GR, Adams RD, O’Dwyer NJ. Reliability of the “Sydney,” “Sunnybrook,” and “House Brackmann” facial grading systems to assess voluntary movement and synkinesis after facial nerve paralysis. Otolaryngol Head Neck Surg. 2005 Apr;132(4):543-9. https://doi.org/10.1016/j.otohns.2005.01.027 Coulson SE Croxson GR Adams RD O’Dwyer NJ Reliability of the “Sydney,” “Sunnybrook,” and “House Brackmann” facial grading systems to assess voluntary movement and synkinesis after facial nerve paralysis Otolaryngol Head Neck Surg 2005 04 132 4 543 549 https://doi.org/10.1016/j.otohns.2005.01.027 20 20. Yen TL, Driscoll CL, Lalwani AK. Significance of House-Brackmann facial nerve grading global score in the setting of differential facial nerve function. Otol Neurotol. 2003 Jan;24(1):118-22. https://doi.org/10.1097/00129492-200301000-00023 Yen TL Driscoll CL Lalwani AK Significance of House-Brackmann facial nerve grading global score in the setting of differential facial nerve function Otol Neurotol 2003 01 24 1 118 122 https://doi.org/10.1097/00129492-200301000-00023 21 21. Guntinas-Lichius O, Klussmann JP, Schroeder U, Quante G, Jungehuelsing M, Stennert E. Primary parotid malignoma surgery in patients with normal preoperative facial nerve function: outcome and long-term postoperative facial nerve function. Laryngoscope. 2004 May;114(5):949-56. https://doi.org/10.1097/00005537-200405000-00032 Guntinas-Lichius O Klussmann JP Schroeder U Quante G Jungehuelsing M Stennert E Primary parotid malignoma surgery in patients with normal preoperative facial nerve function: outcome and long-term postoperative facial nerve function Laryngoscope 2004 05 114 5 949 956 https://doi.org/10.1097/00005537-200405000-00032 22 22. Vrabec JT, Backous DD, Djalilian HR, Gidley PW, Leonetti JP, Marzo SJ, et al. Facial Nerve Grading System 2.0. Otolaryngol Head Neck Surg. 2009 Apr;140(4):445-50. https://doi.org/10.1016/j.otohns.2008.12.031 Vrabec JT Backous DD Djalilian HR Gidley PW Leonetti JP Marzo SJ et al Facial Nerve Grading System 2.0 Otolaryngol Head Neck Surg 2009 04 140 4 445 450 https://doi.org/10.1016/j.otohns.2008.12.031 23 23. Infante-Cossio P, Prats-Golczer VE, Lopez-Martos R, Montes-Latorre E, Exposito-Tirado JA, Gonzalez-Cardero E. Effectiveness of facial exercise therapy for facial nerve dysfunction after superficial parotidectomy: a randomized controlled trial. Clin Rehabil. 2016 Nov;30(11):1097-107. https://doi.org/10.1177/0269215515617309 Infante-Cossio P Prats-Golczer VE Lopez-Martos R Montes-Latorre E Exposito-Tirado JA Gonzalez-Cardero E Effectiveness of facial exercise therapy for facial nerve dysfunction after superficial parotidectomy: a randomized controlled trial Clin Rehabil 2016 11 30 11 1097 1107 https://doi.org/10.1177/0269215515617309 24 24. Ross BG, Fradet G, Nedzelski JM. Development of a sensitive clinical facial grading system. Otolaryngol Head Neck Surg. 1996 Mar;114(3):380-6. https://doi.org/10.1016/S0194-5998(96)70206-1 Ross BG Fradet G Nedzelski JM Development of a sensitive clinical facial grading system Otolaryngol Head Neck Surg 1996 03 114 3 380 386 https://doi.org/10.1016/S0194-5998(96)70206-1 25 25. Yanagihara N. Grading of facial palsy. Proceedings of the Third International Symposium on Facial Nerve Surgery. In: Fisch U, ed. Facial nerve surgery. Amstelveen, The Netherlands: Kugler Medical Publications, 1977. p. 533-5. Yanagihara N Grading of facial palsy. Proceedings of the Third International Symposium on Facial Nerve Surgery Fisch U ed Facial nerve surgery Amstelveen, The Netherlands Kugler Medical Publications 1977 533 535 26 26. Stodulski D, Skorek A, Mikaszewski B, Wiśniewski P, Stankiewicz C. Facial nerve grading after parotidectomy. Eur Arch Otorhinolaryngol. 2015 Sep;272(9):2445-50. https://doi.org/10.1007/s00405-014-3196-y Stodulski D Skorek A Mikaszewski B Wiśniewski P Stankiewicz C Facial nerve grading after parotidectomy Eur Arch Otorhinolaryngol 2015 09 272 9 2445 2450 https://doi.org/10.1007/s00405-014-3196-y 27 27. Moran CJ, Neely JG. Patterns of facial nerve synkinesis. Laryngoscope. 1996 Dec;106(12 Pt 1):1491-6. https://doi.org/10.1097/00005537-199612000-00009 Moran CJ Neely JG Patterns of facial nerve synkinesis Laryngoscope 1996 12 106 12 Pt 1 1491 1496 https://doi.org/10.1097/00005537-199612000-00009 28 28. Nichols RD, Stine PH, Bartschi LR. Facial nerve function in 100 consecutive parotidectomies. Laryngoscope. 1979 Dec;89(12):1930-4. https://doi.org/10.1288/00005537-197912000-00005 Nichols RD Stine PH Bartschi LR Facial nerve function in 100 consecutive parotidectomies Laryngoscope 1979 12 89 12 1930 1934 https://doi.org/10.1288/00005537-197912000-00005 29 29. Davis RA, Anson BJ, Budinger JM, Kurth LR. Surgical anatomy of the facial nerve and parotid gland based upon a study of 350 cervicofacial halves. Surg Gynecol Obstet. 1956 Apr;102(4):385-412. Davis RA Anson BJ Budinger JM Kurth LR Surgical anatomy of the facial nerve and parotid gland based upon a study of 350 cervicofacial halves Surg Gynecol Obstet 1956 04 102 4 385 412 30 30. Baker DC, Conley J. Avoiding facial nerve injuries in rhytidectomy. Anatomical variations and pitfalls. Plast Reconstr Surg. 1979 Dec;64(6):781-95. https://doi.org/10.1097/00006534-197912000-00005 Duplicata da 8 Baker DC Conley J Avoiding facial nerve injuries in rhytidectomy. Anatomical variations and pitfalls Plast Reconstr Surg 1979 12 64 6 781 795 https://doi.org/10.1097/00006534-197912000-00005 Duplicata da 8 31 31. Nason RW, Binahmed A, Torchia MG, Thliversis J. Clinical observations of the anatomy and function of the marginal mandibular nerve. Int J Oral Maxillofac Surg. 2007 Aug;36(8):712-5. https://doi.org/10.1016/j.ijom.2007.02.011 Nason RW Binahmed A Torchia MG Thliversis J Clinical observations of the anatomy and function of the marginal mandibular nerve Int J Oral Maxillofac Surg 2007 08 36 8 712 715 https://doi.org/10.1016/j.ijom.2007.02.011 32 32. Batstone MD, Scott B, Lowe D, Rogers SN. Marginal mandibular nerve injury during neck dissection and its impact on patient perception of appearance. Head Neck. 2009 May;31(5):673-8. https://doi.org/10.1002/hed.21013 Batstone MD Scott B Lowe D Rogers SN Marginal mandibular nerve injury during neck dissection and its impact on patient perception of appearance Head Neck 2009 05 31 5 673 678 https://doi.org/10.1002/hed.21013 33 33. Møller MN, Sørensen CH. Risk of marginal mandibular nerve injury in neck dissection. Eur Arch Otorhinolaryngol. 2012 Feb;269(2):601-5. https://doi.org/10.1007/s00405-011-1610-2 Møller MN Sørensen CH Risk of marginal mandibular nerve injury in neck dissection Eur Arch Otorhinolaryngol 2012 02 269 2 601 605 https://doi.org/10.1007/s00405-011-1610-2 34 34. Ellingson TW, Cohen JI, Andersen P. The impact of malignant disease on facial nerve function after parotidectomy. Laryngoscope. 2003 Aug;113(8):1299-303. https://doi.org/10.1097/00005537-200308000-00006 Ellingson TW Cohen JI Andersen P The impact of malignant disease on facial nerve function after parotidectomy Laryngoscope 2003 08 113 8 1299 1303 https://doi.org/10.1097/00005537-200308000-00006 35 35. Bron LP, O’Brien CJ. Facial nerve function after parotidectomy. Arch Otolaryngol Head Neck Surg. 1997 Oct;123(10):1091-6. https://doi.org/10.1001/archotol.1997.01900100065009 Bron LP O’Brien CJ Facial nerve function after parotidectomy Arch Otolaryngol Head Neck Surg 1997 10 123 10 1091 1096 https://doi.org/10.1001/archotol.1997.01900100065009 36 36. Eviston TJ, Yabe TE, Gupta R, Ebrahimi A, Clark JR. Parotidectomy: surgery in evolution. ANZ J Surg. 2016 Mar;86(3):193-9. https://doi.org/10.1111/ans.13212 Eviston TJ Yabe TE Gupta R Ebrahimi A Clark JR Parotidectomy: surgery in evolution ANZ J Surg 2016 03 86 3 193 199 https://doi.org/10.1111/ans.13212 37 37. Jackson GL, Ballantyne AJ. Role of parotidectomy for skin cancer of the head and neck. Am J Surg. 1981 Oct;142(4):464-9. https://doi.org/10.1016/0002-9610(81)90376-7 Jackson GL Ballantyne AJ Role of parotidectomy for skin cancer of the head and neck Am J Surg 1981 10 142 4 464 469 https://doi.org/10.1016/0002-9610(81)90376-7 38 38. Plopper C, Cernea CR, Ferraz AR, Dos Santos LR, Regis AB. Parotidectomy for primary nonparotid diseases. Otolaryngol Head Neck Surg. 2004 Oct;131(4):407-12. https://doi.org/10.1016/j.otohns.2004.02.053 Plopper C Cernea CR Ferraz AR Santos LR Regis AB Parotidectomy for primary nonparotid diseases Otolaryngol Head Neck Surg 2004 10 131 4 407 412 https://doi.org/10.1016/j.otohns.2004.02.053 39 39. Hong TS, Kriesel KJ, Hartig GK, Harari PM. Parotid area lymph node metastases from cutaneous squamous cell carcinoma: implications for diagnosis, treatment, and prognosis. Head Neck. 2005 Oct;27(10):851-6. https://doi.org/10.1002/hed.20256 Hong TS Kriesel KJ Hartig GK Harari PM Parotid area lymph node metastases from cutaneous squamous cell carcinoma: implications for diagnosis, treatment, and prognosis Head Neck 2005 10 27 10 851 856 https://doi.org/10.1002/hed.20256 40 40. Nakamura Y, Teramoto Y, Asami Y, Imamura T, Sato S, Tanaka R, et al. The rate of facial nerve dysfunction and time to recovery after intraparotid and extraparotid facial nerve exposure and protection in head and neck cutaneous tumor surgery. Int J Clin Oncol. 2017 Oct;22(5):843-8. https://doi.org/10.1007/s10147-017-1148-4 Nakamura Y Teramoto Y Asami Y Imamura T Sato S Tanaka R et al The rate of facial nerve dysfunction and time to recovery after intraparotid and extraparotid facial nerve exposure and protection in head and neck cutaneous tumor surgery Int J Clin Oncol 2017 10 22 5 843 848 https://doi.org/10.1007/s10147-017-1148-4 41 41. 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 Apr;116(4):534-40. https://doi.org/10.1097/01.mlg.0000200741.37460.ea 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 04 116 4 534 540 https://doi.org/10.1097/01.mlg.0000200741.37460.ea 42 42. O’Brien CJ, Petersen-Schafer K, Papadopoulos T, Malka V. Evaluation of 107 therapeutic and elective parotidectomies for cutaneous melanoma. Am J Surg. 1994 Nov;168(5):400-3. https://doi.org/10.1016/S0002-9610(05)80084-4 O’Brien CJ Petersen-Schafer K Papadopoulos T Malka V Evaluation of 107 therapeutic and elective parotidectomies for cutaneous melanoma Am J Surg 1994 11 168 5 400 403 https://doi.org/10.1016/S0002-9610(05)80084-4