Original Article Analysis of Preoperative Factors ... · affected facial nerve in a large number of clinical cases, although to different extents, and provide the possibility of the
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Original Article
Analysis of Preoperative Factors InfluencingHypoglossal-facial ‘Side’-to-side Neurorrhaphy forFacial Paralysis after Excision of Acoustic Neuroma*
SU Di Ya1,2, WAN Hong1, LI De Zhi3, QIAO Hui1, SCHUMACHER Michael4, and LIU Song1,3,4,#
1. Beijing Neurosurgical Institute and Beijing Key Laboratory of Central Nervous System Injury, Capital MedicalUniversity, Beijing 100070, China; 2. Dalian University Affiliated Xinhua Hospital, Dalian 116000, Liaoning,China; 3. Department of Neurosurgery and China National Clinical Research Center for Neurological Diseases,Beijing Tiantan Hospital, Capital Medical University, Beijing 100070, China; 4. U 1195, INSERM and UniversityParis-Sud and University Paris Saclay, 94276 Le Kremlin-Bicêtre, France
Abstract
Objective Hypoglossal nerve-facial nerve ‘side’-to-side neurorrhaphy is a new method for thetreatment of potential incomplete facial paralysis after acoustic neuroma. However, there aredifferences in postoperative outcomes among patients. This study analysed preoperative factors thatmay influence the treatment outcomes of neurorrhaphy.
Methods We performed a retrospective study of 53 patients who were treated by neurorrhaphy forfacial paralysis after acoustic neuroma resection. After a one-year follow-up period, the patients weredivided into two groups according to facial functional outcome: better recovery or ordinary recovery.We analysed the following factors: gender, age, tumour size, and characteristics, tumour adhesion tothe facial nerve, the duration of facial paralysis (DFP) and F wave appearance prior to neurorrhaphy (Fwave).
Results Univariate analysis showed significant differences between the two groups in DFP (P = 0.0002),tumour adhesion to the facial nerve (P = 0.0079) and F waves (P = 0.0048). Logistic regression analysis ofthese factors also showed statistical significance with P values of 0.042 for the DFP, 0.043 for F waves,and 0.031 for tumour adhesion to the facial nerve.
Conclusions Tumour adhesion to the facial nerve, F waves appearance and DFP prior to neurorrhaphyare the predominant factors that influence treatment outcomes.
F acial nerve injury is one of the maincomplications following the surgicalremoval of acoustic neuroma at the
cerebellopontine angle area[1]. When treating facialnerve injury, end-to-end neurorrhaphy between thefacial nerve stumps is the most effective method withregard for the recovery of facial natural function and
the axonal regrowth pathway. However, thisapproach is impossible in most cases because it isoften not feasible to regain the proximal stump of theinjured facial nerve. Thus, other facial dynamicreanimation methods that use the nerve transferringtechnique have been employed with the aim ofoffering alternative sources of axons to innervate thedenervated facial muscles; these include using thehypoglossal nerve, spinal accessory nerve, and
*This work was supported by grants from the National Natural Science Foundation of China [No.81471239].#Correspondence should be addressed to LIU Song, MD, PhD, Tel: 86-18311025866, E-mail: [email protected] note of the first author: SU Di Ya, MD, female, born in 1987, majoring in nerve injury and repair.
30 Biomed Environ Sci, 2020; 33(1): 30-36
masseteric nerve[2,3]. Among the nerves used, thehypoglossal nerve, as a nerve donor, has its ownadvantages for such purposes. Because it provides asufficient axonal source and more powerful facialreanimation even if the hypoglossal nerve is onlyhemisectioned for neurorrhaphy, the existing sharedinnervation of the facial and hypoglossal nuclei withinthe brainstem allows intense facial exercises and therebypromotes central plasticity and facilitates thedevelopment of new functions for hypoglossalmotoneurons to improve facial function[4] and preventsynkinesis of the doubly innervated facial muscles[5-7].In neurosurgery, the development of microsurgicaltechniques allows us to anatomically conserve theaffected facial nerve in a large number of clinicalcases, although to different extents, and provide thepossibility of the patient’s facial nerve recovering onits own. The definition of this condition is potentialincomplete facial paralysis, the incidence of which isrelatively higher in patients with facial nerve injury[8,9].For treating these patients, we improved the classicmethod of hypoglossal-facial end-to-endneurorrhaphy with ‘side’-to-side neurorrhaphy withthe aim of preserving the facial nerve withoutcompromising the remnant axons and allowing thepossibility of spontaneous recovery[10]. A mainoutcome is the double innervation of paralyzed facialmimic muscles by both hypoglossal and facialmotoneurons. However, in clinical practice, we haveobserved variability among patients treated withfacial functional recovery after ‘side’-to-sideneurorrhaphy. Because all neurorrhaphy procedureswere performed by the same neurosurgeon and withthe same and standardized method, we suspect thatpreoperative factors would have major influence ontreatment outcomes.
In this study, we retrospectively assessed 53patients who were treated with hypoglossal nerve-facial ‘side’-to-side neurorrhaphy for facial paralysisresulting from acoustic neuroma resection but withanatomical preservation of the injured facial nerve inour neurosurgical department. Possible preoperativeinfluencing factors were collected and analysed. Weused univariate and logistic analyses to analyse theimpacts of these factors on postoperative functionaloutcomes and to obtain useful information forclinical practice.
SUBJECTS AND METHODS
This was a retrospective study performed with 53patients who experienced facial paralysis due to theremoval of acoustic tumours and were surgically
treated by hypoglossal-facial nerve ‘side’-to-sideneurorrhaphy in our Department of Neurosurgerybetween June 2011 and September 2016. Theinclusion criteria were as follows: (1) the patientdeveloped facial paralysis after acoustic neuromaresection and had normal nerve function before theoperation, (2) the patient’s age ranged from 16 to 70years old, (3) at least one side of the sural nervefunction was normal, (4) no contraindications forgeneral anaesthesia, and (5) voluntary treatment viahypoglossal-facial ‘side’-to-side neurorrhaphy.Patients who did not meet the above criteria wereexcluded from the study. Before the removal of theacoustic tumour, no facial function deficit wasobserved in any of these patients. After surgery, thepatients developed serious facial paralysis with aHouse-Brackmann (H-B) scale grade V or VI, eventhough their facial nerve was anatomically preservedduring tumour removal. The patients were followed-up for one year after the neurorrhaphy. This studywas approved by the local Ethics Committee ofBeijing Tiantan Hospital, Capital Medical University,China (KY2017-006-02).
Neurorrhaphy Treatment
The principal indication for hypoglossal-facialnerve ‘side’-to-side neurorrhaphy was significantincomplete facial paralysis due to facial nerve injury.The preservation of facial nerve anatomical structureafter injury could allow some remnant facial axons tobe conserved and/or lead to spontaneousregeneration. The standard hypoglossal-facial nerve‘side’-to-side neurorrhaphy was performed using apredegenerated nerve autograft (PSNG) in eachpatient by the same neurosurgeon[11]. The use of aPSNG was based on the aim of improving axonalregeneration given the proliferation of its Schwanncells due to axotomies. This concept has beendemonstrated in previous studies by otherinvestigators as well as our own study[11]. Briefly, thesurgical operation was performed under generalanaesthesia. The ipsilateral hypoglossal nerve wasexposed and identified using an electrostimulatorwhile recording the active potential in the tonguemuscle at the ipsilateral side through two insertedelectrodes[12]. One half of the hypoglossal nerve wascross-sectioned at a site closely distal to thedescending branch. The proximal extremity of thePSNG that was predegenerated one week prior toneurorrhaphy and removed from the ipsilateral suralnerve was surgically bridged end-to-‘side’ to thehypoglossal nerve at the partial cross-section site.The injured facial nerve was exposed from its main
Effects of preoprative factors on hypoglossal-facial neurorrhaphy 31
trunk to the bifurcation area as well as its two mainbranches within the parotid gland. An epineuriumwindow was created using microsurgical scissors onthe exposed facial nerve at each of the two mainbranches closely caudal to the bifurcation whilecarefully preserving the tissue structure. The distalextremity of the PSNG was divided into two endsthat were then surgically bridged to the facial nerve,end-to-side, at each of the epineurium windows.Figure 1 illustrates the hypoglossal-facial nerve‘side’-to-side neurorrhaphy. All patients underwentintense rehabilitation exercise after neurorrhaphy.
Clinical Data
The clinical data of the 53 patients are shownabove. Tumour-related clinical data were obtainedfrom detailed surgical records of acoustic neuromaresection. Patients were included in the study onlywhen their surgical record regarding the acoustic
neuroma resection was complete and detailed.Among the included patients, 29 were female and 23were male. The patients’ ages ranged from 19 to 68years old with a mean ± standard deviation (SD) of42.47 ± 13.18 years old. In the clinic, we followed thetraditional route of repair and generallyrecommended patients undergo 3−6 months ofobservation after facial paralysis. The period fromthe onset of facial paralysis to the neurorrhaphyranged from 1 to 84 months with a mean ± SD of12.86 ± 16.26 months (only one patient insisted onundergoing the surgery 1 month after facialparalysis). To obtain accurate results, we did notexclude these data from calculations of significantdifferences. We further divided the patients into 3subgroups according to the duration of facialparalysis to analyse the time pointsat whichneurorrhaphy was performed. The patients weredivided into short (≤ 6 months), medium (7−12months) or long (≥ 13 months) period groups.According to the records, a solid tumour was foundin 34 patients, and tight adhesion between thetumour and facial nerve was observed in 35 patients.The greatest tumour diameters ranged from 1.5 to6.0 cm with a mean ± SD of 4.00 ± 1.10 cm. Beforeneurorrhaphy, electrophysiological examination wasperformed using electromyography (Nicolet EDX,VIASYS Health Care Inc., Madison, Wisconsin, USA)to detect F wave appearances in all patients. F wavesare one of the late responses produced by theantidromic activation of motoneurons viasupramaximal stimulation of the nerve trunk andindicates nerve conduction from the motoneuroncell body to the motor endplate, which has apersistence of typically 80%–100% (or at least above50%) in intact muscles[13]. We found 19 patients withpositive and 34 with negative responses for F waves.The H-B facial nerve scale was used as the mainindicator to assess facial function SupplementaryTable S1 (available in www.besjournal.com).
Statistical Analysis
Age, the duration of facial paralysis and thegreatest tumour diameter are expressed as themean ± SD. GraphPad Prism 6.02 software was usedfor single-factor statistical analysis and one-wayANOVA. Continuous variables such as age, theduration of facial paralysis and greatest tumourdiameter were analysed byunpaired T test. Otherfactors, including, F wave appearance, tumouradhesion to the facial nerve and tumourcharacteristics, were binary variables and wereanalysed by the chi-squared test. SPSS 19.0 software
External auditory canal
Facial n.
PSNG
Mastoid
Hypoglossal n.
Sec�on 50%
Digastric muscle
Figure 1. Schematic drawings showinghypoglossal nerve-facial nerve ‘side’-to-sideneurorrhaphy using a predegenerated nerveautograft (PSNG). One-half of the hypoglossalnerve was cross-sectioned at a site closelydistal to the descendens hypoglossi. Theproximal extremity of the PSNG was surgicallybridged end-to-‘side’ to the hypoglossal nerveat the partial cross-section site. An epineuriumwindow was created using microsurgicalscissors on the exposed facial nerve at each ofthe two or three main branches with carefulpreservation of tissue structure. The distalextremity of the PSNG was divided into twoends that were then surgically bridged to thefacial nerve, end-to-side, at each of theepineurium windows.
32 Biomed Environ Sci, 2020; 33(1): 30-36
was used for logistic statistical analysis. P values ≤0.05 were considered statistically significant. For thelogistic statistical analysis, separate odds ratios (ORs)and 95% CIs were also calculated. In addition, thepatients were also divided into three subgroupsaccording to the duration of facial paralysis forneurorrhaphy timing analysis. The three subgroupswere analysed by one-way ANOVA followed byTukey’s posthoc test for between-groupcomparisons.
RESULTS
Analysis of Preoperative Clinical Data UsingUnivariate Analysis
In this study, 36/53 patients showed betterrecovery of facial function, and 17/53 patientsshowed ordinary recovery. Clinical data wereanalysed using univariate analysis to determinewhich preoperative factors influenced treatmentprognosis after neurorrhaphy.
The age distributions were 41.69 ± 2.19 years oldin the better recovery group and 44.35 ± 3.37 yearsold inthe ordinary recovery group. There wasnosignificant difference between the two groups (P =0.50). There was also no significant differencebetween the two groups (P = 0.57) in the genderdistribution. The duration of facial paralysis beforeneurorrhaphy significantly differed between thebetter recovery group (9.29 ± 0.81 months) and theordinary recovery group (24.24 ± 6.01 months; P =0.0002). In the better recovery group, 25 patientshad solid tumours, and 11 patients had cystictumours. In the ordinary recovery group, 9 patientshad solid tumours, and 8 patients had cystictumours. No significant difference was establishedbetween the two groups intumour characteristics (P= 0.24). However, tumour adhesion to the facialnerve was observed in 19/36 patients in the betterrecovery group and in 16/17 patients in the ordinarygroup (P = 0.0079). A significant difference was also
found between the two groups in F wave recordings(P = 0.0048). Before neurorrhaphy, 18/36 patientshad positive F waves in the better recovery group. Incontrast, only 1/17 patients had a positive F waveresponse in the ordinary recovery group.
Analysis of Preoperative Clinical Data UsingLogistic Regression Analysis
Univariate analysis of the duration of facialparalysis, F wave appearance and tumour adhesionto the facial nerve revealed significant differencesbetween the better recovery and ordinary recoverygroups. These factors were further analysed bylogistic regression analysis, as shown in Table 1. TheP values of the logistic regression analysis were0.042 for the duration of facial paralysis (OR = 1.129,95% CI = 1.004–1.270), 0.043 for F wave appearance(OR = 0.095, 95% CI = 0.010–0.924), and 0.031 fortumour adhesion to the facial nerve (OR = 0.063,95% CI = 0.005–0.779), indicating that theyinfluenced neurorrhaphy treatment prognoses.
The Timing of Performing Neurorrhaphy
Patients were divided into subgroups based onfacial paralysis duration: 26/53 in the short-periodsubgroup, with facial paralysis durations of 4.54 ±1.24 months ( ≤ 6 months); 12/53 in the medium-period subgroup with facial paralysis durations of9.92 ± 1.98 months (7–12 months); and 15/53 in thelong-period subgroup with facial paralysis durationsof 29.67 ± 22.76 months ( ≥ 13 months). Statisticalanalysis performed using one-way ANOVA followedby Tukey’s post hoc test was performed according tothe postoperative functional recovery of H-B gradeand showed that there were significant differencesamong the three subgroups (P ≤ 0.0001). Uponanalysis of the sets of two subgroups �(Figure 2), asignificant difference was established between theshort- and long-period subgroups (P < 0.0001),although there was no difference between the short-and medium-period subgroups (P = 0.053) orbetween the medium- and long-period subgroups
Table 1. Logistic regression analysis results for neurorrhaphy
Variable Unit P value Odds ratio 95% CI
FPD month 0.042 1.129 1.004–1.270
F wave on EMG before the procedure yes/No 0.043 0.095 0.010–0.924
Adhesion between the tumour and facial nerve yes/No 0.031 0.063 0.005–0.779
Note. P values were determined by logistic test.
Effects of preoprative factors on hypoglossal-facial neurorrhaphy 33
(P = 0.111).
DISCUSSION
Both internal and external factors have beenshown to influence the treatment prognosis afterhypoglossal-facial nerve ‘side’-to-side neurorrhaphyfor incomplete facial paralysis resulting from theremoval of acoustic tumour at the cerebellopontineangle area[14,15]. In this study, the surgicalneurorrhaphy procedure was considered aninvariant factor for the extent of facial functionrecovery as the surgeries were performed by thesame neurosurgeon with the same method. Wefound that tumour adhesion to the facial nerve, theduration of facial paralysis and F wave appearanceprior to neurorrhaphy played much more importantroles in treatment prognosis than was found for theother preoperative factors, indicating that both thepreservation of facial axons and theirmicroenvironment are pivotal for postoperativefacial function recovery after ‘side’-to-sideneurorrhaphy[16,17].
Preservation of the anatomical structure of thefacial nerve was a prerequisite for the patients
enrolled in this study, as confirmed by a review ofsurgical recordings after removing their acoustictumour as well clinical and electrophysiologicalevaluations. Based on our clinical experience,patients who underwent facial nerve injury withpreservation of anatomical structure can have someremnant and/or spontaneously regenerated facialaxons even though they experienced complete facialparalysis during the early period after injury thatmay have persisted for several months.
Hypoglossal-facial nerve ‘side’-to-sideneurorrhaphy can effectively preserve facial nervefibres and promote double innervation of theparalyzed facial muscles by both hypoglossal andfacial motoneurons[8,11]. The concept of side-to-sideneurorrhaphy was introduced by Dr. Terzis in 1984as a part of the ‘babysitter’ procedure for facialreanimation[18]. Since then, few studies havereported using side-to-side neurorrhaphy to treatfacial paralysis, particularly in cases with significantincomplete facial paralysis with hypoglossal-facialnerve side-to-side neurorrhaphy. However, thedisadvantages of this technique potentially includethat it requires two coaptation sites between thehypoglossal and facial nerve when using a nervegraft, and this is likely to reduce the number ofregenerated axons that enter the repaired facialnerve, most likely because scar formation at thecoaptation sites obstruct the passage of theregenerating axons and lead to axonal escaping fromthe sites and a longer pathway for axonal elongation.These points remain to be further investigated.Limitations of the study may include eintrinsic andextrinsic factors related to nerve regenerationabilities, which are most likely related to the patient’s psychological state and quality, individual physicalconditions, the extent of intensive postoperativefacial exercise, large variation in age, and otherunknown factors.
After ‘side’-to-side neurorrhaphy, theparticipation of facial axons in postoperativefacial functional recovery involves the remnantand/or spontaneous regeneration of axons within theoriginal facial nerve pathway. Undoubtedly, tumouradhesion to the facial nerve results in nerve damageduring its removal at the cerebellopontine anglearea, which occurs inproportion to the� amount oftumour adhesion[1,8,19]. Thus, careful preservation ofthe facial nerve or restoration of the anatomiccontinuity when the nerve is sectioned duringremoval of the acoustic tumour is very important forthe postoperative prognosis. In addition, F waveappearance prior to neurorrhaphy is an effective
Short
≤ 6 mMedium7−12 m
Long
≥ 13 m
****4
3
2
1
0
Grad
es im
prov
ed fr
om H
-B sc
ale
Figure 2. Statistical analysis was performedusing one-way ANOVA followed by Tukey’spost-hoc test according to the postoperativefunctional recovery on the H-B scale, and theresults showed that there were significantdifferences among the three subgroups (****P ≤0.001). Upon analysis of sets of two subgroups(Figure 2), a significant difference wasestablished between the short- and long-period subgroups (P < 0.001), although therewas no difference between the short- andmedium-period subgroups (P = 0.053) orbetween the medium-and long-periodsubgroups (P = 0.111).
34 Biomed Environ Sci, 2020; 33(1): 30-36
indicator of the extent of nerve damage[20].Double innervation of facial muscles by both
hypoglossal and facial axons may result in thereliable restoration of resting facial symmetry andtone. Their innervation by hypoglossal motoneuronsallows powerful movement, whereas reinnervationby facial motoneurons improves physiologicalrecovery[21]. In addition, the incidence of synkinesismaybe reduced if the facial muscles are innervatednot only by transposed hypoglossal axons but also byremnant and/or spontaneous regenerating facialaxons. Indeed, shared innervation of facial musclesby the motoneurons of the facial and hypoglossalbrainstem nuclei may prevent synkinesis[5-7,22]. Therespective contribution of remnant facial axons andregenerated hypoglossal axons to facial functionalrecovery and the underlying mechanisms remain tobe investigated.
The delay between facial palsy and nervereconstruction is referred to as facial paralysisduration and has also been found to be an importantfactor for functional recovery. The duration of facialparalysis may result in unfavourable changes in theaxonal microenvironment within the facial nerve.During prolonged facial paralysis, Schwann celltubules within the distal nerve stump and motorendplates progressively degenerate and may evendisappear, whereas distal target muscles undergoatrophy[23-25]. Moreover, the functionalreorganization of central nervous systemsensorimotor areas after long-term facial paralysisalso plays an important role in functional recovery,particularly after nerve transfer treatmentperformed using an ectopic axonal source[26-28].
Therefore, we stress that early facial nerve repairis necessary to achieve a better functional recovery.In this study, the best results were obtained inpatients who had experienced facial paralysis for lessthan 6 months without any apparent facial muscleatrophy. These results are consistent with the workof Guntinas-Lichius et al.[29], who showed that adenervation period not exceeding 112 d allowedbetter functional recovery after facial nerve injury.We thus propose that hypoglossal-facial nerve ‘side’-to-side neurorrhaphy should be performed as earlyas possible in patients with significant facial nerveinjury if the absence of spontaneous innervation isobserved within 3 months after the onset of facialparalysis[30].
CONCLUSION
In this study, we reviewed 53 patients who
experienced facial nerve injury due to the removalof an acoustic tumour at the cerebellopontineangle area and then underwent hypoglossal-facialnerve ‘side’-to-side neurorrhaphy to treatsignificant facial paralysis in our neurosurgicaldepartment from June 2011 to September 2016. Toanalyse the impact of factors evaluated prior toneurorrhaphy on the postoperative recovery offacial function, we assessed preoperative factors,including gender, age, tumour size andcharacteristics, tumour adhesion to the facialnerve, the duration of facial paralysis and F waveappearance, using univariate as well as logisticanalyses. We found that tumour adhesion to thefacial nerve, F wave appearance and the durationof facial paralysis prior to neurorrhaphy are thepredominant factors that influence neurorrhaphytreatment outcomes. Tumour adhesion to thefacial nerve and F wave appearance are indicatorsof the extent of facial nerve injury, whereas theduration of facial paralysis affects themicroenvironment in the nerve distal stump andtarget muscles, suggesting that the carefulpreservation of the facial nerve and earlyneurorrhaphy are very important for treatmentoutcomes.
ACKNOWLEDGEMENTS
The authors thank Ms. WANG Ming Ran and LIPing (Beijing Neurosurgical Institute) for theirexcellent assistance in the electrophysiologicalevaluations.
DISCLOSURE
The authors report no conflicts of interestconcerning the materials or methods used in thisstudy or the findings specified in this paper.
Received: March 20, 2019;Accepted: December 4, 2019
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