7
SURGICAL ONCOLOGY AND RECONSTRUCTION Lingual Nerve Repair: To Graft or Not to Graft? Michael Miloro, DMD, MD, * Phil Ruckman III, DDS,y and Antonia Kolokythas, DDS, MScz Purpose: Since no studies have compared direct and graft repair of the lingual nerve, we examined the subjective and objective outcomes of lingual nerve repair by direct epineurial repair and indirect graft repair, assessed the effect of other confounding variables, and compared the outcomes of autograft and allograft repairs. Patients and Methods: All patients who had undergone microneurosurgical repair of the lingual nerve from 2000 to 2012 by 1 surgeon (M.M.) were asked to complete an online questionnaire regarding their current neurosensory status at least 2 years after nerve repair. A direct comparison was made between patients who had undergone direct epineurial repair and those who had undergone interpositional nerve graft repair. Student’s t test and c 2 test were used to determine whether a significant difference existed in the success between the 2 techniques and whether age, gender, race, delay from injury to repair, or degree of initial nerve deficit influenced the success of nerve repair. Results: Of the 72 patients identified, 43, who had undergone 47 nerve repairs (18 direct, 29 indirect graft repairs [4 bilateral]; 28 female and 19 male patients; mean age 28.3 years), were interviewed. The objective results of functional sensory recovery, defined by a Medical Research Council Scale grade of S3, S3+, or S4, was 89% for the graft repairs and 85% for the direct repairs (P = .01). The subjective patient satisfaction score (0 to 10 scale) was 8.9 for the graft repairs and 8.1 for the direct repairs (P = .02). The autograft and allograft repairs performed comparably, and the other variables (ie, age, gender, race, delay from injury to nerve repair, gap length, and initial Sunderland grade injury) were not found to be significant (P > .05). Conclusion: Graft repair of the lingual nerve provides superior long-term (>2 years) objective and subjective outcomes compared with direct repair. This might be because of the lack of tension at the repair site, more freedom with nerve stump preparation, and the addition of neurotropic and neurotrophic factors from the donor nerve graft at the site of injury to augment neurosensory recovery. Ó 2015 American Association of Oral and Maxillofacial Surgeons J Oral Maxillofac Surg 73:1844-1850, 2015 Third molar extractions are the most common cause of injury to the inferior alveolar (IAN) and lingual (LN) nerves owing to the proximity of the nerves in the area. 1 However, treatment of pathologic lesions, orthognathic surgery, maxillofacial trauma, local anesthetic injection, endodontic therapy, and dental implant placement have also been implicated as etiologic factors in trigeminal nerve injuries. 2-5 After a nerve injury, proper documentation with clinical neurosensory testing is imperative to determine whether and when microneurosurgical intervention is warranted. 6 Ideally, nerve repair, when indicated, should be performed within 1 to 3 months after the initial injury for the LN and 3 to 6 months for the IAN. Received from Department of Oral and Maxillofacial Surgery, University of Illinois at Chicago College of Dentistry, Chicago, IL. *Professor and Head. yChief Resident. zAssociate Professor and Program Director. Conflict of Interest Disclosures: Dr Miloro is a Consultant for Axo- Gen, Inc, Alachua, FL. Address correspondence and reprint requests to Dr Miloro: Department of Oral and Maxillofacial Surgery, University of Illinois at Chicago College of Dentistry, 801 S Paulina St, Chicago, IL 60612; e-mail: [email protected] Received February 11 2015 Accepted March 5 2015 Ó 2015 American Association of Oral and Maxillofacial Surgeons 0278-2391/15/00268-2 http://dx.doi.org/10.1016/j.joms.2015.03.018 1844

Lingual Nerve Repair: To Graft or Not to Graft?

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SURGICAL ONCOLOGY AND RECONSTRUCTION

Rec

Un

Ge

De

Lingual Nerve Repair:To Graft or Not to Graft?

eived

iversity

*Profes

yChiefzAssociConflic

n, Inc, A

Addres

partme

Michael Miloro, DMD, MD,* Phil Ruckman III, DDS,yand Antonia Kolokythas, DDS, MScz

Purpose: Since no studies have compared direct and graft repair of the lingual nerve, we examined the

subjective and objective outcomes of lingual nerve repair by direct epineurial repair and indirect graftrepair, assessed the effect of other confounding variables, and compared the outcomes of autograft and

allograft repairs.

Patients andMethods: All patients who had undergone microneurosurgical repair of the lingual nervefrom 2000 to 2012 by 1 surgeon (M.M.) were asked to complete an online questionnaire regarding their

current neurosensory status at least 2 years after nerve repair. A direct comparison was made between

patients who had undergone direct epineurial repair and those who had undergone interpositional nerve

graft repair. Student’s t test and c2 test were used to determine whether a significant difference existed in

the success between the 2 techniques and whether age, gender, race, delay from injury to repair, or degree

of initial nerve deficit influenced the success of nerve repair.

Results: Of the 72 patients identified, 43, who had undergone 47 nerve repairs (18 direct, 29 indirect

graft repairs [4 bilateral]; 28 female and 19 male patients; mean age 28.3 years), were interviewed. The

objective results of functional sensory recovery, defined by a Medical Research Council Scale grade of

S3, S3+, or S4, was 89% for the graft repairs and 85% for the direct repairs (P = .01). The subjective patientsatisfaction score (0 to 10 scale) was 8.9 for the graft repairs and 8.1 for the direct repairs (P = .02). The

autograft and allograft repairs performed comparably, and the other variables (ie, age, gender, race, delay

from injury to nerve repair, gap length, and initial Sunderland grade injury) were not found to be significant

(P > .05).

Conclusion: Graft repair of the lingual nerve provides superior long-term (>2 years) objective and

subjective outcomes comparedwith direct repair. This might be because of the lack of tension at the repair

site, more freedom with nerve stump preparation, and the addition of neurotropic and neurotrophic

factors from the donor nerve graft at the site of injury to augment neurosensory recovery.

� 2015 American Association of Oral and Maxillofacial Surgeons

J Oral Maxillofac Surg 73:1844-1850, 2015

Third molar extractions are the most common causeof injury to the inferior alveolar (IAN) and lingual

(LN) nerves owing to the proximity of the nerves in

the area.1 However, treatment of pathologic lesions,

orthognathic surgery, maxillofacial trauma, local

anesthetic injection, endodontic therapy, and dental

implant placement have also been implicated as

from Department of Oral and Maxillofacial Surgery,

of Illinois at Chicago College of Dentistry, Chicago, IL.

sor and Head.

Resident.

ate Professor and Program Director.

t of Interest Disclosures: Dr Miloro is a Consultant for Axo-

lachua, FL.

s correspondence and reprint requests to Dr Miloro:

nt of Oral and Maxillofacial Surgery, University of Illinois

1844

etiologic factors in trigeminal nerve injuries.2-5 After anerve injury, proper documentation with clinical

neurosensory testing is imperative to determine

whether and when microneurosurgical intervention is

warranted.6 Ideally, nerve repair, when indicated,

should be performed within 1 to 3 months after the

initial injury for the LN and 3 to 6 months for the IAN.

at Chicago College of Dentistry, 801 S Paulina St, Chicago, IL

60612; e-mail: [email protected]

Received February 11 2015

Accepted March 5 2015

� 2015 American Association of Oral and Maxillofacial Surgeons

0278-2391/15/00268-2

http://dx.doi.org/10.1016/j.joms.2015.03.018

FIGURE 2. Diagram of indirect (graft) nerve repair technique.

Miloro, Ruckman, and Kolokythas. Lingual Nerve Repair. J OralMaxillofac Surg 2015.

MILORO, RUCKMAN, AND KOLOKYTHAS 1845

Diagnostic imaging of the trigeminal nerve remains in

the developmental stages, with magnetic resonance

neurography showing the most promise in the ability

to distinguish a neuroma from normal nerve tissue in

the LN and IAN.7-9 Therefore, the clinical examination

(subjective and objective testing) remains the

mainstay of diagnosis and treatment planning. The

indications for microneurosurgery include completepostoperative anesthesia, observed nerve transection,

and minimal residual sensation, which is typically

seen with Sunderland grade III, IV, and V injuries.10

Nerve repair can be performed using a direct epi-

neurial repair (Fig 1) or an indirect (graft) neurorrha-

phy procedure (Fig 2), using a graft if tension is

perceived at the nerve repair site. The 2 options for

graft repair include autogenous nerve grafts (auto-grafts) and allogeneic nerve grafts (allografts). The

most appropriate autogenous nerve graft for the

trigeminal nerve is the sural nerve because of the

diameter and fascicular pattern match with the

trigeminal nerve anatomy.11 Only 1 allograft is

available, the Avance nerve graft (available in a variety

of diameters and lengths; AxoGen, Inc, Alachua, FL).

In considering the outcomes of direct versus graftrepair, conventional thinking has maintained that a

direct repair would result in a greater likelihood of

recovery than a grafted repair owing to the increased

length of nerve regeneration required from the cell

body to the target site through the graft and the need

for 2 sites of epineurial anastomosis with the potential

for 2 separate sites of fascicular misalignment (poor

coaptation), 2 sites of potential axonal microsproutingoutside the epineurium, and 2 sites of nerve scarring

that could impede neural regeneration.12

The overall success rates of microneurosurgery of

the trigeminal nerve have varied considerably in the

published data from 26 to 92%,13 and subjective

success has not always correlated with objective

improvement.14 Additionally, standardization in the

reported studies of trigeminal nerve repair regardingsuccessful outcomes, as defined by functional (or

useful) sensory recovery according to the Medical

Research Council Scale (MRCS), is lacking.15

Although many studies have reported individual

FIGURE 1. Diagram of direct epineurial nerve repair technique.

Miloro, Ruckman, and Kolokythas. Lingual Nerve Repair. J OralMaxillofac Surg 2015.

surgeon experience with trigeminal nerve repair,

no study has evaluated the difference in the success

of direct versus indirect repair techniques for the

trigeminal nerve.

Patients and Methods

After approval by the University of Illinois institu-

tional review board (IRB no. 2013-1098), the Common

Procedural Terminology codes for trigeminal nerverepair (codes 64716, 64727, 64864, and 64885) were

used to search for nerve repair cases completed by 1

surgeon (M.M.) from April 2000 to December 2012,

with at least 2 years of follow-up data after the nerve

repair procedure. The patient demographic informa-

tion was taken from a retrospective medical record

review and evaluation of the clinical notes. Once the

subject was identified, the patient was interviewedby telephone (P.R.) and asked for a valid e-mail address.

The subject was e-mailed a link to complete a

20-question online survey (Survey Monkey, Palo Alto,

CA) and a consent form to access their individual

written or electronic medical record (EMR) for age,

gender, race, type of nerve repair, and information

regarding the neurologic examination at the initial

presentation before the nerve repair and at thefollow-up examinations. The results of the question-

naire and the data from the EMRs were analyzed for

significance, specifically comparing the direct and

indirect nerve repair techniques. Student’s t test and

the c2 test were used to determine whether a signifi-

cant difference existed in the success between the 2

techniques and whether age, gender, race, gap length,

degree of initial nerve deficit (Sunderland grade), andtype of nerve graft (autograft vs allograft) influenced

the outcomes of the nerve repair.

Subjective neurosensory recovery was evaluated by

individual patient responses to the subjective survey

questions, and the objective questions of neurosen-

sory recovery were correlated with the MRCS, with

grades S3, S3+, and S4 indicating the presence of

functional (or useful) sensory recovery (FSR).16 AnFSR score of S3 corresponds to a return of some

superficial pain and tactile sensation without over-

response and 2-point discrimination of >15 mm

(Table 1).17

Table 1. MEDICAL RESEARCH COUNCIL SCALE

Grade* Description

S0 No sensation

S1 Deep cutaneous pain in autonomous zone

S2 Some superficial pain and touch

S2+ Superficial pain and touch plus hyperesthesia

S3 Superficial pain and touch without hyperesthesia:

static 2-point discrimination >15 mm

S3+ Same as S3 with good stimulus localization; static

2-point discrimination of 7-15 mm

S4 Same as S3; static 2-point discrimination of

2-6 mm

* Grades S3, S3+, and S4 indicate functional (useful) sensoryrecovery.13

Miloro, Ruckman, and Kolokythas. Lingual Nerve Repair. J OralMaxillofac Surg 2015.

1846 LINGUAL NERVE REPAIR

Results

Patient data were available for 43 of the 72 patients

(65.3%). Of the 43 patients, 25 were female (58.1%)

and 18 were male (41.9%), and the mean age of the

43 patients was 28.3 years (range 17 to 52). These

demographic data are consistent with other studies

with regard to the risk factors for lingual nerve injury,including advanced age and female gender.18 A total

of 47 LN repairs were performed in the 43 patients,

including 19 direct epineurial repairs (40.4%) and 28 in-

direct repairs (4 bilateral graft repairs) (59.6%). Of the

28 graft repairs, 24 were sural nerve autografts

(85.7%) and 4 were Avance (AxoGen) allografts

(14.3%). Three of the bilateral cases were repaired

with a sural nerve graft, and 1 patient was treatedwith a bilateral Avance nerve graft. The median interval

between nerve injury and repair was 3.2months (range

0.75 to 16.4). The etiology of nerve injury was third

molar odontectomy in 34 of 43 patients (79%),

followed by pathologic excision in 5 (12.0%), orthog-

nathic surgery in 3 (7.0%), and dental implants in 1

(2.0%). Of the LN injuries, 29 were right-sided

(61.7%) and 18 were left-sided (38.3%). The Sunder-land19 grades of initial nerve injury included 1 Sunder-

land grade II, 5 Sunderland grade III, 18 Sunderland

grade IV, and 23 Sunderland grade V injuries using stan-

dard clinical neurosensory testing.20 Another 2 cases of

LN injury were explored, and the patients underwent

external neurolysis without the need for direct or indi-

rect neurorrhaphy, and these patients were excluded

from the study group of 47 repairs. These 2 cases mighthave represented injection-related injuries to the

LN.21,22 Of the patients in the present study, all had

hypoesthesia or anesthesia, but none had symptoms

of neuropathic pain before surgery or after surgical

repair.23 In addition, a trend was observed such that

the patients who experienced improved outcomes

after LN repair also reported on the questionnaire

that the sural nerve harvest site was not a significant

cause of unpleasant symptoms or concern or signifi-

cant hypoesthesia or dysesthesia.11 An additional

finding was that the outcomes of the 4 bilateral cases

were comparable to those of the unilateral cases

(>80% subjective and objective satisfaction), and theinjuries and intraoperative findings were consistent

within the patients with bilateral injuries. All 4 patients

with bilateral injuries presented with bilateral Sunder-

land grade V injuries due to third molar removal by

non–oral and maxillofacial surgeons, and the intraoper-

ative findings were consistent with complete transec-

tion in all cases bilaterally. Finally, 3 of the 4 bilateral

cases received sural nerve autografts and did not reportsignificant sural deficit or morbidity.11

All surgical procedures were performed by 1 sur-

geon (M.M.) with the assistance of residents in training

in oral and maxillofacial surgery. The surgeries were

performed with loupe magnification (3.5� power),

and a standard subperiosteal approach to the LN was

used to identify the proximal and distal nerve seg-

ments and then working toward the site of injury.24

Notation was made of the condition of the injured

nerve, and this was correlated with the preoperative

clinical neurosensory testing results and Sunderland

classification.20

The preoperative clinical neurosensory testing was

grouped into 1 of 5 categories (Sunderland I, normal

[n = 0]; Sunderland II, mild injury [n = 1]; Sunderland

III, moderate injury [n = 5]; Sunderland IV, severeinjury [n = 18]; Sunderland V, complete injury, [n =

23]). The intraoperative findingswere also categorized

into 5 groups (normal/intact in 0, compressed/intact

in 2, neuroma-in-continuity in 5, partial transection

in 18, and complete transection in 22). A fairly good

linear correlationwas found between the preoperative

neurosensory testing results and the condition of the

LN observed at nerve repair, with only 1 degree ofdifference in 5 cases (Fig 3). Next, the area of injury

was addressed by resection of the visible neuroma

and sequential resection of 1- to 2-mm segments of

both proximal and distal nerve stumps to visualize

healthy axoplasm with vascularity to ensure that no

neuroma remained in either the proximal or distal

nerve stumps. At this point, a subjective clinical deter-

mination was made regarding whether the resultantnerve gap length (mean gap length 1.6 mm for direct

repairs and 14.3 mm for gap repairs) could be reap-

proximated with blunt proximal and distal nerve

stump dissection and release (into the pterygomandib-

ular space proximally and into the floor of the mouth

distally). On occasion, a single epineurial suture was

placed to visualize howmuch tension would be placed

on the repair site with direct epineurial repair. If it

FIGURE 4. A, Intraoperative view of a direct epineurial left lingual nervnerve repair with an autogenous sural nerve graft (note, 2 sites of neurorr

Miloro, Ruckman, and Kolokythas. Lingual Nerve Repair. J Oral Maxillo

FIGURE 3. Scatter plot representing the relationship between thepreoperative sensory impairment score and the severity of lingualnerve injury identified at nerve repair (n = 47 nerves). C/I, com-pressed/intact; CT, complete transection; N/I, normal/intact;NIC, neuroma-in-continuity; PT, partial transection.

Miloro, Ruckman, and Kolokythas. Lingual Nerve Repair. J OralMaxillofac Surg 2015.

MILORO, RUCKMAN, AND KOLOKYTHAS 1847

were determined that the proximal and distal nerve

stumps could not lie in direct apposition without a

gap between the segments that would result in undue

tension on epineurial repair, the decision was made to

use a nerve graft for repair (Fig 4).

Before 2008, all grafts were performed using a sural

nerve (medial sural cutaneous nerve from the sacral

plexus S1-S2) graft.11 However, since then, most graftshave been performed using a cadaveric nerve allograft

(Avance, AxoGen), typically, 2 to 3 mm or 3 to 4mm in

diameter, depending on the recipient nerve, with the

length ranging from 10 to 30 mm, depending on the

gap length for the LN.25,26 In addition, nerve

protectors, consisting of porcine small intestine

submucosa (AxoGuard, Axogen), were used with the

allografts at the proximal and distal neurorrhaphysites to prevent axonal microsprouting and prevent

adherence and scarring to the surrounding soft

tissues during healing (Fig 5).

The objective results of functional sensory recovery,

defined by a Medical Research Council System score

e repair. B, Intraoperative view of an indirect epineurial left lingualhaphy).

fac Surg 2015.

FIGURE 5. A, Intraoperative view of an indirect epineurial right lingual nerve repair with an allograft (Avance, AxoGen). B, Nerve protectors(AxoGuard, AxoGen) in place to protect the 2 sites of neurorrhaphy repair.

Miloro, Ruckman, and Kolokythas. Lingual Nerve Repair. J Oral Maxillofac Surg 2015.

1848 LINGUAL NERVE REPAIR

of S3, S3+, or S4, was 89% for the graft repairs and 85%

for the direct repairs. The subjective patient satisfac-

tion score (0 to 10 scale) was 8.9 for the graft repairs

and 8.1 for the direct repairs (Fig 6). These differences

were statistically significant for both the objective out-

comes (P = .01) and subjective outcomes (P = .02). Inaddition, an evaluation of the other variables,

including age, gender, race, interval from injury to

repair, gap length, and initial Sunderland grade of

injury were not significant in terms of objective and

subjective patient outcomes (P > .05).

Discussion

Studies on the outcomes of trigeminal nerve repair

have focused on the cumulative results of both LN

and IAN repair, mostly from individual surgeon experi-

ence, and the surgical reports have included a mixture

of direct and indirect repair procedures.27-33 To date,

no study has evaluated the difference in subjective

and objective outcomes between direct and indirecttrigeminal nerve repair techniques.

The general assumption is that a direct repair should

perform better than a grafted nerve repair for many rea-

FIGURE 6. A, Objective outcomes functional sensory recovery after direafter direct (8.1) and graft (8.9) repairs (P = .02).

Miloro, Ruckman, and Kolokythas. Lingual Nerve Repair. J Oral Maxillo

sons. First, to qualify for a direct repairwithout tension,

the gap defect must be small. Therefore, themagnitude

of injury to the nerve (ie, size of the neuroma) would

likely need to be small, with minimal Wallerian degen-

eration, and, would thus have an improved chance of

recovery after surgical repair. Pogrel34 suggested thatearly repairs might have less neuroma formation and

therefore require less resection and a lower chance

of requiring a nerve graft and a better prognosis for re-

covery. Pogrel34 suggested that direct repair has

improved outcomes compared with graft repair,

although he did not compare the outcomes of direct

versus graft repair (most of the ‘‘grafts’’ were vein graft

conduits). In contrast, perhaps in an attempt to avoidthe additional morbidity of nerve graft harvest or

because of a lack of surgeon expertise in graft harvest-

ing, less than adequate resection of neuromatous tissue

could be a compromised intraoperative decision,

which would certainly result in worse outcomes by

leaving neuroma in the nerve stumps (and performing

a neuroma-to-neuroma repair) rather than abandoning

the neurorrhaphy procedure completely. In addition,in an attempt to avoid a nerve graft, perhaps more ten-

sion than ideally desired (ideal tension is no tension)35

ct (81%) and graft (89%) repairs (P = .01). B, Subjective outcomes

fac Surg 2015.

MILORO, RUCKMAN, AND KOLOKYTHAS 1849

could be present at the repair site, resulting in vascular

compromise, poor healing, and scar formation at the

anastomosis site. Another theoretical reason that direct

repairs should perform better than graft repairs is that

there is only 1 site of neurorrhaphy (nerve suture anas-

tomosis) instead of the 2 sites in graft repair. This

would result in a lower risk of fascicular adaptation

(coaptation) mismatch (at 1 site vs 2 sites) and wouldalso lessen the chance of collateral axonal microsprout-

ing outside the epineurium at the repair site by 50%

(Fig 2). Finally, with a smaller amount of neuroma

resection and a minimal, or no, nerve gap with a direct

repair, anterograde and retrograde axonal transport

across the repair site should occur more readily and

rapidly from the cell body to the target site in a direct

repair versus a graft repair.However, the factors that favor an improved

outcomewith graft repair compared with direct repair

include the ability of the surgeon to resect neuroma-

tous tissue both proximally and distally with impunity,

but only to the certain point at which additional nerve

resection will not permit neurorrhaphy owing to the

inability to access the proximal and/or distal nerve

stumps. This ‘‘surgical freedom’’ would permit animproved chance of reaching normal healthy fascic-

ular tissue (well-vascularized mushrooming axoplasm)

in both the proximal and the distal nerve stumps. Also,

an additional benefit of using a nerve graft is the ability

to bring healthy nerve tissue, alongwith the associated

potent neurotropic and neurotrophic factors, to a site

of injury to augment recovery after repair.36,37 This is

true of both autografts and allografts, although theprimary goal of the graft is the transfer of the

fascicular conduit architecture that will accept and

guide the proximal regenerating nerve sprouts

toward the distal nerve stump and target site.

Although many studies have shown a lack of corre-

lation between objective and subjective testing of

neurosensory function,38 this present study showed

a correlation between the 2 assessments, likelybecause the patient questionnaire was completed by

the patient for both the subjective and the objective

questions, with the known limitation of the study

being that objective clinical neurosensory testing by

an experienced clinician was not possible owing to

the various locations of the patients and their inability

to travel for a formal follow-up examination. In addi-

tion, the lack of significance of the interval from injuryto repair conflicts with the results of some previous

studies.39 However, this might have resulted from

aggressive resection to healthy fascicular tissue, which

was a critical consideration in the present study, and

the threshold for considering nerve graft repair was

very low. Therefore, any additional scar tissue forma-

tion or Wallerian degeneration of the nerve stumps

as a result of an increased interval from injury to repair

was likely not a significant factor in the outcomes of

our study, because it was aggressively resected.

In conclusion, the present study has documented

that indirect graft nerve repair, using an autograft

(sural nerve) or allograft (Avance nerve graft) is

associated with improved objective and subjective

nerve outcomes compared with direct nerve repair.

Surgeons who perform microneurosurgical repair ofthe trigeminal nerve must recognize the importance

of resection of all neuromatous tissue and a tension-

free repair on achieving successful outcomes. Also,

they must be capable of performing nerve graft repair,

with either harvest of an autograft or the use of a stock

allograft. To further determine appropriate evidence-

based decisions and treatment recommendations for

patients who sustain injuries to the terminal branchesof the trigeminal nerve, including the LN and IAN, a

prospective multicenter, multisurgeon clinical trial is

warranted, because the last attempt at such a study

more than 2 decades ago, had significant limitations.40

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