Comparison of the Effects of Neural Mobilization and

Arousal Facilitation Protocol in Patients with Prolonged

Disorders of Consciousness
Shaoyang Zhang

Zhejiang University School of Medicine First Affiliated Hospital

Lingxiu Sun
Zhejiang University School of Medcine,Liangzhu Branch
ZiQiang Yang
Zhejiang Rehabilitation hospital
Lijuan Cheng
Hangzhou Normal University
YuQing Dai
Hangzhou Normal University
Xue Lin
Hangzhou Normal University
Yingxuan Hu
Hangzhou Normal University
Zuobing Chen
Zhejiang University School of Medicine First Affiliated Hospital
Steven Laureys
University of Liege: Universite de Liege
Daming Wang
Zhejiang University School of Medicine First Affiliated Hospital
Haibo Di
Hangzhou Normal University

Research Article

Keywords: Prolonged Disorders of Consciousness, Unresponsive Wakefulness Syndrome, Minimally Conscious

State, Neural Mobilization, CRS-R

Posted Date: August 28th, 2024

DOI: https://doi.org/10.21203/rs.3.rs-4731958/v1

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License:   This work is licensed under a Creative Commons Attribution 4.0 International License. Read Full
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Abstract
(1)Background: Patients with severe brain injuries who are bedridden for extended periods often exhibit
diminished voluntary movements. This reduction can compromise the precision of CRS-R evaluations. The
Arousal Facilitation Protocol (AFP)is designed to extend the duration of patient arousal through deep muscle
pressure. Conversely, Neural Mobilization (NM) seeks to augment nerve activity post-brain injury and encourages
the resurgence of voluntary movements. The study aims to identify effective strategies for enhancing
consciousness levels in DoC patients by comparing the efficacy of AFP and NM.

(2) Methods: Fifty-one DoC patients, who met the inclusion criteria, were evaluated by therapist using AFP and
NM in a randomized sequence for CRS-R and BRS-Hand. The assessment results of both groups were then
statistically analyzed. (3) Results: Among the 51 study patients, 12 (23.5%) showed differences in consciousness
diagnosis. Results indicated statistical differences between the AFP and NM groups in diagnosis, total CRS-R
score, visual, auditory, motor subscales, and BRS-Hand score (P<0.05). Further investigation demonstrated that
patients in the AFP group with higher motor subscale scores showed a more pronounced trend of diagnostic
changes in the NM group (P=0.045).

(4) Conclusion: The NM approach exhibits superior efficacy in enhancing the diagnosis of patient consciousness
in DoC, promoting the restoration of conscious behavior, and improving hand function, compared to AFP.
Supplementation of NM with the CRS-R scale can help increase the level of consciousness of pDoC.

Trial registration: ChiCTR, ChiCTR2200056285. Registered 3 February 2022,

https://www.chictr.org.cn/ChiCTR2200056285

1. Introduction
Patients with severe brain injuries caused by traumatic brain injury, cerebrovascular and cardiovascular diseases,
among other reasons, may transition into Disorders of Consciousness after experiencing a period of coma
(1).Disorders of consciousness include coma (unwakefulness, reflex behaviours only), unresponsive wakefulness
syndrome (previously known as vegetative state; wakefulness but reflex behaviours only) and minimally
conscious state (clinical demonstration of signs of consciousness)(2) (3, 4). MCS is further subdivided into MCS-
(demonstrating non-reflexive behaviors but without language comprehension) and MCS+ (possessing language
comprehension ability) (5), DOC lasting over four weeks is defined as Prolonged DoC (pDoC)(6). To promote
consensus, the Coma Recovery Scale-Revised (CRS-R) is recommended as a standardized assessment tool(2, 7,
8).

These patients often suffer severe disabilities, rely on others long-term, and burden families and society. Accurate
assessment of DoC patients' consciousness level is crucial for treatment(9–11). DoC patients often experience
fatigue and fluctuations in arousal, making assessment challenging. To prolong arousal, the CRS-R scale requires
the use of an Arousal Facilitation Protocol: present deep pressure stimulation unilaterally to the face, neck,
shoulder, and sternocleidomastoid muscles(12). As the disease progresses, prolonged bed rest and
immobilization may lead to complications such as motor dysfunction and sensory impairment, ultimately
reducing the expression of conscious behavior and compromising the accuracy of assessment(9). Therefore,
exploring more effective methods to enhance patient arousal and consciousness expression is crucial.

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Research shows that brain injuries often lead to neural axis damage, causing mobility loss and severe
consequences. Long-term abnormal postures and immobilization, related to elevated CNS tension, hinder
voluntary movement recovery (13, 14). Neural mobilization, based on neurodynamic principles, aims to influence
neural structures and their environment through manual techniques or exercises, providing important methods
for clinical assessment and treatment, especially in cases of neural involvement or mechanical sensitivity (15,
16). Studies have shown that median nerve electrical stimulation facilitates consciousness recovery in patients
with coma and chronic disorders of consciousness(17–19). Therefore, neural mobilization of the upper
extremities, especially the median nerve, can alleviate tension abnormalities and promote conscious behavior
recovery.

This study aims to enhance the responsiveness of DoC patients during CRS-R assessment. By comparing AFP
and NM as arousal-enhancing methods, statistical analysis was conducted to evaluate the specific impact of
neural mobilization techniques on CRS-R scores and hand motor recovery.

2. Materials and Methods

① Inclusion criteria

Patients aged over 18 years; duration of illness > 28 days; chronic disorder of consciousness patients with stable
vital signs.

② Exclusion criteria

Upper extremity skin or joint pathologies (e.g., wounds, bedsores, or fractures); pre-existing upper extremity
functional disability; bilateral muscle tone with MAS over 3.

Methodology: Before the assessment, it was ensured that patients were not administered any sedative
medications. Each patient underwent two evaluations within one hour by an experienced therapist: one using the
AFP and the other replacing it with neural mobilization before CRS-R and BRS-hand assessments. The order was
randomized. Scores were analyzed using SPSS 25.0, with P < 0.05 indicating statistical significance.

Neural mobilization (all passive movements): 1. With the patient in a supine position, shoulder abduction is
conducted under passive movement. During elbow extension, wrist dorsiflexion is incrementally increased to
achieve full, comfortable abduction and arm extension. 2. Under passive movement, the elbow is flexed with the
wrist in palmar flexion. Gradual elbow extension accompanies forearm pronation, followed by arm abduction, full
elbow extension, and maintained forearm pronation. 3. With passive movement, the wrist is dorsiflexed while the
elbow remains flexed. Gradual elbow extension and forearm supination occur, culminating in simultaneous arm
abduction when the elbow is fully extended and supinated.

Assessment Tools

The CRS-R is considered the authoritative standard for behavioral assessment in DoC patients. This scale
comprises 23 items, covering six dimensions including auditory, visual, motor, communication, oral/verbal
activities, and arousal(12). The Brunnstrom Recovery Stage (BRS) focuses on evaluating hand motor function in
DoC patients. Initially proposed by Brunnstrom in 1966 based on observations of stroke patients, it delineates the
pattern of limb movement recovery post-stroke. Based on the degree of spasticity and the emergence of

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voluntary movements, BRS divides the recovery process into six stages, where higher stages indicate better
motor recovery. This pattern also applies to traumatic brain injury patients(20, 21). In this study, we utilized the
BRS hand scale to quantify the hand motor abilities of DoC patients and observed and scored during the CRS-R
assessment process. See Fig. 1.

3. Results
3.1Data analysis results
A total of 66 patients with severe brain injury were enrolled in Shanghai Yongci Hospital, excluding: age > 80 years
old, n = 1; Irregular vital signs, n = 2; severe upper limb spasms, n = 8; refusal to participate,n = 1; EMCS,n = 2; Post-
injury time < 28 days, n = 1; Finally, 51 patients with DoC were included. Statistical analysis was performed with
IBM SPSS25.0 software. There were 51 patients with DoC, median post-injury time = 238 days, median age = 60
years, 14 males, and 17 with traumatic brain injury(see Table1).

All variables were tested to be non-normally distributed. Of the 51 study patients, 12 (23.5%) showed a difference
in conscious diagnosis. In the AFP group: UWS = 30, MCS:21(MCS-:17, MCS+:4); In the NM group: UWS:21,
MCS:30(MCS-:21, MCS+:9). After Fisher's exact test, the results showed that there were statistically significant
differences between the AFP group and the NM group in diagnosis(p = 0.007). Using Wilccockson's sign rank test,
the results showed that there were statistically significant differences between the AFP group and the NM group
in the CRS-R total score (p < 0.001), visual (p = 0.014), auditory (p = 0.041), motor subscale (p = 0.024) and BRS
left\right hand scores(p < 0.001), see Figure. 2.

A comparative analysis between two groups, each consisting of 12 patients with and without diagnostic
discrepancies, revealed a significant correlation. Higher scores on the motor subscale in the AFP group were
associated with an increased likelihood of diagnostic changes in the NM group (P = 0.045).
3.2. Figures, Tables and Schemes

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 Table 1
Clinical data of patients in UWS and MCS
Patient Age Gender Etiology time AFP*CRS- NM*CRS- AFP*Diagnosis NM*Diagnosis
after R Total R Total
injury
(days)

1 46 M TBI 269 12 12 MCS- MCS-

2 65 F NTBI 160 10 10 MCS- MCS-

3 66 M TBI 163 13 13 MCS- MCS-

4 66 M TBI 260 11 13 MCS- MCS+

5 70 M TBI 280 10 10 MCS- MCS-

6 51 F TBI 345 10 10 MCS- MCS-

7 75 F NTBI 222 9 11 MCS- MCS+

8 47 F NTBI 333 14 14 MCS- MCS-

9 69 M NTBI 119 6 6 MCS- MCS-

10 25 M TBI 379 14 14 MCS- MCS-

11 75 M NTBI 848 12 12 MCS- MCS-

12 71 M NTBI 289 9 9 MCS- MCS-

13 22 F NTBI 613 9 9 MCS- MCS-

14 66 M TBI 56 6 8 MCS- MCS-

15 63 F NTBI 73 9 9 MCS- MCS-

16 51 M NTBI 149 10 10 MCS- MCS-

17 56 M NTBI 189 10 12 MCS- MCS+

18 71 M TBI 506 13 15 MCS+ MCS+

19 54 F TBI 86 14 14 MCS+ MCS+

20 40 M NTBI 752 13 13 MCS+ MCS+

21 35 M TBI 77 15 15 MCS+ MCS+

22 64 M NTBI 336 6 12 UWS MCS-

23 71 M NTBI 705 7 7 UWS UWS

24 2572 M NTBI 279 6 6 UWS UWS

25 65 M TBI 511 7 10 UWS MCS-

26 71 M NTBI 274 7 9 UWS MCS-

27 29 M TBI 224 7 7 UWS UWS

28 65 F NTBI 1122 5 5 UWS UWS

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 Patient Age Gender Etiology time AFP*CRS- NM*CRS- AFP*Diagnosis NM*Diagnosis
after R Total R Total
injury
(days)

29 60 M NTBI 478 5 5 UWS UWS

30 47 M NTBI 77 5 5 UWS UWS

31 60 F NTBI 57 4 7 UWS MCS+

32 65 M TBI 623 7 7 UWS UWS

33 36 M NTBI 460 4 4 UWS UWS

34 41 F NTBI 474 5 5 UWS UWS

35 37 M NTBI 297 6 6 UWS UWS

36 66 M TBI 490 6 6 UWS UWS

37 81 M NTBI 479 6 9 UWS MCS-

38 43 M NTBI 100 1 1 UWS UWS

39 71 M TBI 298 3 6 UWS MCS-

40 27 F NTBI 51 4 4 UWS UWS

Patient Age Gender Etiology time AFP*CRS- NM*CRS- AFP*Diagnosis NM*Diagnosis

after R Total R Total
injury
(days)

41 43 M NTBI 131 3 3 UWS UWS

42 57 F TBI 58 3 6 UWS MCS+

43 43 M NTBI 35 4 4 UWS UWS

44 65 F NTBI 17 4 6 UWS UWS

45 52 M NTBI 86 7 7 UWS UWS

46 33 M NTBI 111 4 4 UWS UWS

47 65 M NTBI 231 7 9 UWS MCS-

48 64 M NTBI 92 5 8 UWS MCS-

49 69 F TBI 115 6 6 UWS UWS

50 51 M NTBI 127 4 4 UWS UWS

51 47 M NTBI 238 5 5 UWS UWS

4. Discussion
This study compares the effects of NM with the AFP on the CRS-R score and BRS hand score in DoC. The findings
indicate that upper extremity NM results in significantly higher CRS-R and BRS scores than AFP. Our results

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suggest that improving arousal in DoC patients is highly dependent on different stimulation modalities.
Specifically, neurolysis performed along the direction of peripheral nerves proves to be more effective in
promoting conscious behaviors, particularly auditory, visual, and motor-related behavioral expressions, than deep
pressure stimulation aimed at enhancing sensory stimulation.

In recent years, to enhance the accuracy and sensitivity of the CRS-R scale, personalized recommendations have
been proposed(9, 22–26). Research indicates that employing mirrors, calling patients' names, using items of
interest to patients, and conducting repeated assessments can enhance patient responsiveness. In this study, 12
patients (23.5%) with DoC showed improved awareness of their diagnosis. The NM group effectively enhanced
the consciousness level of these patients. The nervous system is connected, and damage to any part can affect
others, highlighting its interconnected nature(13). Existing research has demonstrated that even without self-
initiated movement of the torso, the movement of the limbs can stretch the structures within the neural canal(27),
Specifically, during elbow and wrist extension, the median nerve experiences a 20% increase in length compared
to when it is in a flexed position(13). Stretching peripheral nerves and nerve roots can enhance their influence on
the spinal cord, brainstem, and cerebral cortex. Cooper et al. discovered that median nerve electrical stimulation
(MNES) significantly enhances arousal in patients with disorders of consciousness, reduces ICU stay, and
accelerates speech recovery. The stimulated group also demonstrated greater improvements in functional
independence and quality of life. Further analysis revealed that patients with higher motor subscale scores under
the Assessment of Prognosis (AFP) are more likely to experience an upgrade in consciousness diagnosis after
MNES, suggesting that neural mobilization may effectively increase arousal and promote consciousness
expression by mobilizing the median nerve(18, 28).

This study demonstrated significant statistical differences between the NM and AFP groups in visual, auditory,
motor subscales, and BRS hand scores. Consistent with prior research, 282 patients with MCS were observed,
yielding the five most prevalent conscious behaviors derived from visual, auditory, and motor ability
subscales(29). NM significantly enhances arousal, auditory response, and motor ability of patients by influencing
the connection pathway from upper limb peripheral nerves to the brainstem and motor cortex. Hand movement is
intimately linked to the visual control network(30), indicating that nerve loosening in the upper limbs can augment
visual center function and improve visual behavior. While NM did not significantly modify the arousal subscale
score, the patient's eye-opening time increased during the assessment; however, this positive change did not yield
additional points in the CRS-R evaluation.

This study shows that DoC patients with higher motor subscale scores during AFP are more likely to experience
enhanced consciousness diagnosis after NM. Thus, managing hand motor function is crucial for DoC patients.
With up to 60% incidence of severe limb spasticity in DoC patients(31), prolonged sensory deprivation and
abnormal neural tension contribute significantly(32). NM promotes hand motor recovery in DoC patients,
enhancing CRS-R assessment accuracy and serving as an effective therapeutic intervention.

5. Limitation
Our study underscores the advantages and importance of employing neuromobilization in CRS-R. Nonetheless, it
is imperative to acknowledge that patients with severe upper limb spasticity were not included in the study.
Owing to the pandemic, long-term follow-up data on patients are absent. Future research should bolster the
reliability of study conclusions by enlarging the sample size and conducting double-blind randomized controlled
trials, while also increasing follow-up data to evaluate the potential effects of NM in mitigating abnormal muscle
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tone. Furthermore, it is suggested to utilize objective assessment tools such as EEG and EMG to delve deeper
into the effects of NM on the brain and its associated neural pathways.

6. Conclusion
This study demonstrates that NM significantly enhances conscious behavioral expression in patients and
improves the sensitivity of CRS-R assessments. Additionally, NM promotes hand movement recovery, aiding DoC
patients in regaining daily self-care abilities. This is particularly beneficial for patients with potential upper limb
movements who gradually lose activity due to immobilization. Compared to Minimally Conscious State (MCS)
patients, Unresponsive Wakefulness Syndrome (UWS) patients are more prone to misdiagnosis, necessitating
repeated assessments for improved diagnostic accuracy. However, time constraints hinder their clinical
implementation. NM can circumvent increased evaluation time due to repeated measurements, facilitating
clinical application.

Declarations
Competing interests
The authors declare that the research was conducted in the absence of any commercial or financial relationships
that could be construed as a potential conflict of interest.

Funding:
This research was funded by the National Natural Science Foundation of China (Grant no. 81920108023);
Intergovernmental International Science and Technology Innovation Cooperation & Strategic Science and
Technology Innovation Cooperation (Grant no.2022YFE0141300); Key R&D Program of Zhejiang Province grant
number 2022C03038; BLB19J014. Interdisciplinary Research Project of Hangzhou Normal University
(2024JCXK07)

Authors' contributions:
S.Z.: conceptualization, methodology, software, formal analysis, investigation, data curation, writing-original draft,
visualization, funding acquisition. L.S.: software, validation, investigation, data curation, writing-original draft,
visualization. Z.Y.: validation, investigation, data curation, writing review, and editing. L.C.: validation, investigation,
data curation, writing review, and editing. Y.D. and X.L.: validation, investigation, data curation, writing-original
draft, visualization. Y.H.: validation, investigation, data curation, writing review, and editing. Z.C. and S.L.:
supervision, project administration, funding acquisition. D.W. and H.D.: conceptualization, methodology, formal
analysis, writing-review and editing, visualization, supervision, project administration, funding acquisition. All
authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement:

The study protocol was approved by the Ethics Committee of Hangzhou Normal University and Zhejiang
University School of Medicine. It has been registered by the Chinese Clinical Trials Registry (registration number:
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ChiCTR2200056285). The patient’s legal surrogates obtained informed consent.

Data Availability Statement:

All data generated or analyzed during this study are included in this published article [and its supplementary
information files].

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Figures

Figure 1

Flowchart of the study.

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Figure 2

Neural Mobilization(NM) vs The Arousal Facilitation Protocol (AFP) : The differences of CRS-R score and BRS
hand score in AFP group and NM group.

Supplementary Files
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DATA.xlsx

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