PERIPHERAL NERVE SURGERY AND RESEARCH
Cortical Adaptation Staging System
A New and Simple Staging for Result Evaluation of Functioning Free-Muscle
Transplantation for Facial Reanimation
Chieh-Han John Tzou, MD, PhD,*Þ David Chwei-Chin Chuang, MD,* and Hsin-Yu Sirena Chen, MD*
Background: Movement-associated cortical reorganization occurs in patients
after functioning free-muscle transplantation (FFMT), which is reinnervated
by different neurotizers. Aiming to evaluate the process of recovery of the
reinnervated muscle, we defined the cortical reorganization into 5 stages. This
staging system has been applied during the past 25 years at our center with
great convenience and accessibility.
Methods: A standardized evaluation method for assessing the recovery after
FFMT to reanimate the paralyzed face with at least a 1-year follow-up was
applied. The evaluation included the following 5 stages: no movement, de-
pendent movement, independent movement, and spontaneous movement with
and without involuntary movement. Reliability of this technique was assessed
by 3 examiners, who each evaluated the smiles of 30 unilateral facial paralysis
patients 4 times, creating 360 sets of measurements.
Results: The intraclass correlation coefficients for interrater and intrarater
reliability exceeded 0.929, which is considered excellent and reliable.
Conclusions: Chuang’s Cortical Adaptation Staging System is simple, quick,
and accurate in evaluating patients after FFMT reanimation of the paralyzed
face with no additional tools.
Key Words: smile reanimation, fMRI, FFMT, functioning free-muscle
transplantation, free functional-muscle scoring system, facial paralysis, facial
reanimation, facial palsy, cortical adaptation, cerebral adaptation,
neuroplasticity
(Ann Plast Surg 2014;73: 50Y53)
M ovement-associated cortical reorganization occurs when neural
networks in the brain change after a head injury in response to
behavior changes during development in childhood and learning, in
rehabilitation after physical injury such as after amputation with loss
of a limb, in processing sensory reeducation after sensory reinner-
vation, or after functioning free-muscle transplantation (FFMT) which
is reinnervated by a different neurotizer.
Processing sensory information induces neurons in the brain
to sprout to form synapses and restructure the neural pathways. In
addition, frequently used synapses are strengthened, whereas unused
synapses are weakened and eventually eliminated completely. This
cortical reorganization (cortical adaptation) is called neuroplasticity,
or brain plasticity.1,2
Received June 4, 2013, and accepted for publication, after revision, October 23, 2013.
From the *Department of Plastic Surgery, Chang Gung Memorial Hospital, Chang
Gung University, Taoyuan, Taiwan; and †Division of Plastic and Reconstruc-
tive Surgery, Department of Surgery, Medical University of Vienna, Austria.
Conf licts of interest and sources of funding: none declared.
Reprints: David Chwei-Chin Chuang, MD, Department of Plastic Surgery, Chang
Gung Memorial Hospital, Chang Gung University, 5 Fu-Hsing St, Kuei-Shan,
Taoyuan 333, Taiwan. E-mail: dccchuang@gmail.com.
Supplemental digital content is available for this article. Direct URL citations appear
in the printed text and are provided in the HTML and PDF versions of this article
on the journal’s Web site (www.annalsplasticsurgery.com).
Copyright * 2014 by Lippincott Williams & Wilkins
ISSN: 0148-7043/14/7301Y0050
DOI: 10.1097/SAP.0000000000000064
50 www.annalsplasticsurgery.com
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
The phenomenon of cortical adaptation has been observed by
the senior author and others after nerve transfer and FFMT in patients
with brachial plexus injury3Y8 and facial paralysis.9Y11 In addition,
cortical adaptation has been studied by multiple specialties applying
functional magnetic resonance imaging (f MRI).12Y14 However, f MRI
is not the gold standard to stage this long-term process of cortical
adaptation, which usually takes years.
We recently introduced and tested the reliability of Chuang’s
Cortical Adaptation Staging System to evaluate the outcome of 1-stage
smile reconstruction.15,16 This system has been applied in the last
25 years to assess the outcomes after FFMT reconstruction. The aim
of this study was to evaluate the reliability and reproducibility of this
staging system in facial paralysis reconstruction.
MATERIALS AND METHODS
From January 1987 to December 2011, a total of 329 facial
palsy patients with 335 FFMTs for smile reconstruction were
performed. Six patients were reconstructed with bilateral gracilis
muscles to correct Möbius syndrome with bilateral facial paralysis.
All the pertinent surgeries were performed by the same senior sur-
geon (D.C-C.C.). Ninety-nine percent of FFMTs (331/335) used the
gracilis muscle. The remaining cases were pectoralis minor (2 pa-
tients), serratus anterior (1 patient), and rectus femoris (1 patient).
Several different motor nerves were used. A classic 2-stage procedure
with cross-face nerve-graftYinnervated muscle was performed most
commonly (282/329, 85.7%). The XI nerve-innervated muscle was
the second most popular (36/329, 10.9%). Small group of patients
were reconstructed with masseter nerve V3 (4 cases, 1.2%), ipsilat-
eral facial nerve (6 cases, 1.8%), and contralateral facial nerve as 1-
stage procedure (1 case, 0.3%). All enrolled patients were followed
up for at least 1 year. The results were evaluated clinically or using
standardized photographs and video, taken postoperatively at each
visit in the clinic.
Evaluation Technique
The Cortical Adaptation Staging assigned a score from I to V
(Table 1, Fig. 1) to characterize patients’ coordination and activation of
FFMT based on the response after being requested to use the FFMT.
The patient application with this evaluation in this article was focused
only on the patients who had XI-innervated FFMT reconstruction for
facial reanimation. Stage I was given when there was no or little
movement of FFMT in the beginning. If a dependent movement or
smile was seen on the FFMT with movement of the same side of the
shoulder, elevation, or abduction, a stage II was given (video 1, Sup-
plemental Digital Content 1, http://links.lww.com/SAP/A92). Stage III
or independent movement was given when a smile was performed
without the need of shrugging the shoulders (video 2, Supplemen-
tal Digital Content 2, http://links.lww.com/SAP/A93). When a spon-
taneous smile with minimal involuntary movement of the FFMT
could be induced by a tickling test, a stage IV was given (video 3,
Supplemental Digital Content 3, http://links.lww.com/SAP/A94).
Stage V was a spontaneous smile, with no or little involuntary
movement of the FFMT (video 4, Supplemental Digital Content 4,
Annals of Plastic Surgery & Volume 73, Number 1, July 2014
Annals of Plastic Surgery & Volume 73, Number 1, July 2014
TABLE 1. Chuang’s Cortical Adaptation Staging System for
FFMT
Stages Muscle function
Stage I No FFMT movement (or smile)
Stage II Dependent FFMT movement (or smile)
Stage III Independent FFMT movement (or smile)
Stage IV Spontaneous FFMT movement (or smile), with
presence of involuntary movement
Stage V Spontaneous FFMT movement (or smile), without
involuntary movement
http://links.lww.com/SAP/A95, and video 5, Supplemental Digital
Content 5, http://links.lww.com/SAP/A96).
Rehabilitation Program After XI-Innervated Muscle
Transplantation
During clinical evaluation, which usually occurs at 3 to 4
months postoperatively, the examiner is positioned at the same eye
level as the patient. The patient’s face is relaxed and looking straight
ahead. The patient is ordered to smile and then to elevate or abduct
the shoulder (trigger movement) on the same side as the paralyzed
face to see whether the FFMT moved. If any movement of FFMT was
observed when triggered, it was rated stage II for dependent move-
ment. If the FFMT showed no movement, the patient was advised to
enter a rehabilitation program for stimulating the FFMT. The de-
pendent movement would become more and more dominant during
the next 3 to 6 months (7Y9 months postoperatively). Once the trig-
gered FFMT movement became dominant, the patient would be ad-
vised to decrease the trigger movement progressively until it becomes
independent. Stage III or independent movement usually occurred at
6 months postoperatively. After this period, mirror smile training
would be started to achieve a spontaneous smile with less/without
involuntary movement (stage IV/V). The involuntary movements
were unwanted induced movement of the face, when patient smiled,
for example, elevating a limb for putting on clothing, combing the
hair, or scratching the face. Moreover, the patient would be advised to
learn how to control the different degrees of FFMT movement for
small, moderate, and big smiles without shoulder abduction (trigger
movement), also to learn how to adjust the normal side of the face to
cooperate with the FFMT movement on the paralyzed side to achieve
a symmetrical smile. This is called mirror therapy rehabilitation.
Reliability of Chuang’s Cortical Adaptation
Stage System
To evaluate the reliability of Chuang’s Cortical Adaptation Stage
System, 30 adult unilateral facial nerve palsy patients who were re-
constructed with XI-innervated muscle were chosen and evaluated.
Standardized videos of the patients were shown to 3 independent phy-
sician evaluators. To calculate interrater and intrarater reliability of the
cortical adaptation stage, each evaluator rated the patients 4 times, with
an interval of 2 days between each evaluation. Thus, each patient was
rated 12 times to generate a data set of 360 evaluations.
Statistical Analysis
Interrater and Intrarater reliability was determined using
intraclass correlation coefficients (ICCs). Differences among evalu-
ators and different times using the same evaluator were assessed
using the mixed model to demonstrate whether the measurements
changed across patients. P G 0.05 was considered statistically sig-
nificant. Statistical analysis was performed with IBM SPSS software
(IBM Corp, released 2012, IBM SPSS Statistics for Windows,
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Cortical Adaptation Staging System
Version 21.0, Armonk, NY) by the Biostatistical Center for Clinical
Research, Chang Gung Memorial Hospital, Linkou, Taiwan.
RESULTS
Interrater Reliability
The interrater reliability of the measurements was highly accurate,
with an average ICC of 0.929 (excellent) for smile. The overall average
difference of grading between the 4 sets of each patient and among the
observers was 0.05.
Intrarater Reliability
Observer 1 had an ICC of 0.993 and a mean difference among the
4 sets of grading of 0.05. Observer 2 had an ICC of 0.994 and a mean
difference of 0.05 among the 4 sets of grading. Observer 3 had an ICC of
0.994 and a 0.05 mean difference. There were no statistically significant
differences among the 3 observers’ grading (P = 0.173), nor did the
staging scores of each patient change significantly over time (P = 0.335).
DISCUSSION
Induction Exercise
All neurotization patients need ‘‘induction exercise’’ during reha-
bilitation after nerve transfer, with or without FFMT reconstruction.4Y8
Induction exercise is a kind of trigger exercise, like an internal nerve
stimulation. Once the reinnervated muscle stretching is seen or felt, the
induction exercise should start. Different neurotizers have different in-
duction exercises.4,7 A number of exercises are used to induce the
reinnervated muscle to exercise more: after XI nerve transfer, shoulder
raising or shoulder bending back against resistance exercise; after phrenic
or intercostal nerve transfer, running, walking, or climbing hills; after
contralateral C7 spinal nerve transfer, donor limb shoulder-grasping ex-
ercises with resistance. These exercises are kinds of motor reeducation,
which can induce the cortical adaptation progressively. The realization
of the importance of these exercises is crucial, as good results are com-
monly achieved by psychologically strong and ambitious patients who
cooperate well in their rehabilitation programs, whereas poor results are
often obtained by lazy or uncooperative patients.
Five-Stage Grading System
In the early era, the senior author found 5 clinical signs of func-
tional recovery that appear at different times during the postoperative
course after intercostal nerve transfer to the musculocutaneous nerve or
to innervate a FFMT.5 Stage I is the time right after surgery until the
reinnervation of the biceps muscle occurs. Stage II, the dependent phase,
is when the patient can flex the elbow by taking a deep breath (induction
exercise). Stage III, the independent phase, is when the patient can flex
the elbow independently from the respiratory movements. Stages IV and
V, the spontaneous phases, correspond to the status when the patient can
bend the elbow without thinking of breathing but thinking of bending the
elbow. In these stages, the biceps cortical center seems to take control of
elbow flexion by way of the respiratory cortical center through the pe-
ripheral respiratory nerve pathway.17,18
The process of cortical adaptation for intercostal nerve transfer to
the musculocutaneous nerve actually parallels the 5-stage system for smile
reconstruction by FFMT. For the XI-innervated muscle for facial paralysis,
stage I is when the functional muscle is successfully coapted to its recip-
ient motor nerve, but no excursion of the muscle can be detected. After
stage I is the dependent phase, stage II. At this stage, FFMT can be ac-
tivated by the original function of the XI donor nerve. The inducing
movement of facial palsy reanimated with XI-innervated muscle is
shrugging or abducting the shoulders. Gradually, patients enter the inde-
pendent phase of stage III, where they smile without moving their
shoulders. Apparently in stage III, the cortical control center of the smile
makes new neural connections to the spinal accessory nerve and takes
www.annalsplasticsurgery.com 51
Tzou et al Annals of Plastic Surgery & Volume 73, Number 1, July 2014

FIGURE 1. Chuang’s Cortical Adaptation Staging System illustrated by drawings. Stage I, no FFMT movement or smile.
Stage II, dependent FFMT movement or smile. Stage III, independent FFMT movement or smile. Stage IV, spontaneous FFMT
movement or smile with involuntary movement by tickling. Stage V, spontaneous FFMT movement by tickling.

control over the FFMT, and no inducing movement is needed to activate
the FFMT. The last 2 stages (IV and V) are in the spontaneous phase. The
patients can smile spontaneously in funny situations or when they are
tickled. A spontaneous smile with some involuntarily shoulder movements
is classified as stage IV. Stage V is a spontaneous smile with no need of
any shoulder movements. A similar situation will occur in masseter-
innervated muscle or cross-face nerve-graftYinnervated muscle for facial
reanimation, but with different durations of the different stages (Table 2).
Published reports about cortical adaptation show only the
process of brain plasticity after FFMT for smile reconstruction,9,10

52 www.annalsplasticsurgery.com * 2014 Lippincott Williams & Wilkins

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Annals of Plastic Surgery & Volume 73, Number 1, July 2014
TABLE 2. Different Neurotizers With Different Periods of Stages
Stage CFNG-Innervated Muscle
I 6Y12 mo
II 12Y18 mo
III V 6 mo
IV V (sometimes eye blinking on the normal side will 6Y12 mo Involuntary movement decreases over time Biting or chewing will permanently induce
induce FFMT on the paralyzed side twitching)
V After 2 y
CFNG indicates cross-face nerve graft; XI, spinal accessory nerve.
but lag in classifying the stages. Different neurotizer-innervated
muscles have different periods of staging (Table 2). It is crucial to
form an international consensus language to compare FFMT outcome
between different neurotizers. Our objective staging system has been
proved to provide great convenience and accessibility to assess the
phases of cortical adaptation for FFMT, and it offers more effective
therapy for educating patients.
A limitation of the Cortical Adaptation Staging System is
observed clinically when patients are not ticklish. With such patients,
we cannot perform the tickling test, and we have to take more time to
stimulate patients to get into a mood for smiling by telling jokes or
putting them in funny situations. With these efforts, we can check the
existence of a spontaneous smile.
In evaluating the reliability and reproducibility of this staging
system in XI-innervated muscle for facial reanimation, the ICCs for
interrater and intrarater reliability exceeded 0.929, which is consid-
ered excellent and significant. The system should also be valuable in
V3-innervated muscle or cross-face nerve-graftYinnervated muscle-
reconstruction patients.
Science Investigation of the Cortical Adaptation
There are still many unknown frontiers to be explored and
questions to be solved in this newly evolving field. According to
Manktelow et al,10 f MRI cannot be used to study cortical adaptation
of the masseter-innervated FFMT for facial reanimation of the par-
alyzed face because of the close proximity of the ‘‘jaw muscle center/
masseter nerve’’ and ‘‘facial movement center/facial nerve ’’ in the
brain. Further f MRI studies are being prepared at our institution to
investigate the complexity of the mechanism of cortical adaptation in
the field of reconstructive microsurgery with FFMT, especially in the
complex coordinate movement of smiling.
Although showing adaptability of the cerebral cortex de-
teriorates with increasing age10 and apparently follows decreases in
sensory recovery,19 we currently do not have enough patients to draw
a statistically significant conclusion about the age difference or sen-
sory recovery difference which may affect the cortical adaptation.
CONCLUSIONS
Chuang’s Cortical Adaptation Staging System is an objective
grading system, which can serve as a simple, reliable, and accurate tool
for assessing the cortical adaptation process of FFMT. It is easy to fol-
low and practical for clinical routine because it does not require specific
training, complex measurements, calculations, or specialized equipment.
ACKNOWLEDGMENTS
The authors thank research assistants Ms Pei-Ju Chen and Ms
Hsiao-Jung Tseng, MPH, of the Department of Biostatistical Center
for Clinical Research, Chang Gung Memorial Hospital, Taoyuan,
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Cortical Adaptation Staging System
FFMT
XI-Innervated Muscle Masseter-Innervated Muscle
1Y4 mo 1Y2 mo
4Y6 mo 2Y4 mo
4Y6 mo
involuntary movement
Taiwan, for professional and continuous technical assistance throughout
this study and for providing statistical support and analysis of the data.
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