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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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