Sensitive sensory stimulation for the arousal treatment of a persistent vegetative state following traumatic brain injury: a care-compliant case report

Hui-Wen Mao; Yan Li

doi:10.4103/2773-2398.348257

CASE REPORT

Year : 2022 | Volume : 1 | Issue : 2 | Page : 115-121

Sensitive sensory stimulation for the arousal treatment of a persistent vegetative state following traumatic brain injury: a care-compliant case report

Hui-Wen Mao, Yan Li
Department of Rehabilitation Medicine, Shanghai Tongren Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China

Date of Submission	09-Apr-2022
Date of Decision	14-May-2022
Date of Acceptance	23-May-2022
Date of Web Publication	29-Jun-2022

Correspondence Address:
Yan Li
Department of Rehabilitation Medicine, Shanghai Tongren Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai
China

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/2773-2398.348257

Abstract

Effective treatments for patients in a persistent vegetative state due to traumatic brain injury (TBI) are currently unavailable. The purpose of this study was to investigate the therapeutic use of sensitive sensory stimulation for patients in persistent vegetative state following TBI. This case report discussed a 36-year-old male patient who experienced TBI 75 days prior to admission. Upon hospital admission, the patient was unconscious, could automatically open his eyes, but could not avoid light, trace motions, or execute commands. He was placed on a nasal feeding diet, exhibited urinary and fecal incontinence and developed postoperative urinary retention and a pulmonary infection. He showed no mobility of the upper and lower extremities with hypomyotonia. Medications for nerve repair, regaining consciousness, preventing seizure, resolving phlegm, and protecting the stomach were administered. The activity of the extremities was improved by exercise therapies and low or medium-frequency electric stimulation, bladder and bowel function was improved by acupuncture and abdominal massage, and consciousness recovery was promoted by acupuncture and hyperbaric oxygen therapy. Five months following admission, the patient regained consciousness with improved bladder and bowel function. Electroencephalogram indicated that brain function had significantly improved. Auditory evoked potentials and somatosensory evoked potentials suggested that sensation conduction pathways had improved significantly. Sensitive sensory stimulation in combination with routine rehabilitation treatment can effectively cause the regain of consciousness in patients with persistent vegetative state following TBI and improve activities of daily living and the function of the sensation conduction pathways..

Keywords: arousal treatment; coma; electroencephalogram; persistent vegetative state; sensitive sensory stimulation; somatosensory evoked potential; traumatic brain injury

How to cite this article:
Mao HW, Li Y. Sensitive sensory stimulation for the arousal treatment of a persistent vegetative state following traumatic brain injury: a care-compliant case report. Brain Netw Modulation 2022;1:115-21

How to cite this URL:
Mao HW, Li Y. Sensitive sensory stimulation for the arousal treatment of a persistent vegetative state following traumatic brain injury: a care-compliant case report. Brain Netw Modulation [serial online] 2022 [cited 2023 Jun 7];1:115-21. Available from: http://www.bnmjournal.com/text.asp?2022/1/2/115/348257

Funding: The study was supported by the Science and Technology Department of Jiangxi Province Project (Nos. 20212BAG70023, 20202BBG72002) and the Health Commission of Jiangxi Province Project (Nos. 20204202, 2019A117).

Introduction

Brain injury is a leading cause of disability in industrialized and developing countries worldwide (Post et al., 2015). Approximately 69 million people experience traumatic brain injury (TBI) each year, and the incidence of TBI in China is 55.4–64.1 per 100,000 (Dewan et al., 2018). It was predicted that TBI will become one of the primary causes of death and disability by 2020 (Azouvi et al., 2017), further imposing an extensive burden on families and society. Brain injury patient mortality rates have gradually decreased with the continuous development of medical technology. Although patients with severe brain injury awaken from acute coma, they often cannot recover self and environmental awareness (Tang et al., 2017). Persistent vegetative state (PVS) is caused by a loss of cortical function following severe injury to the cerebral hemispheres, while the brainstem function remains relatively intact, leading to a subcortical survival syndrome. The loss of self and environmental consciousness can persist for ≥ 1 month, and this state is considered the most negative outcome in patients with severe head injury besides death. PVS severely affects the quality of life of patients and their caretakers and causes additional medical and societal issues and concerns (Song et al., 2018). Medical therapies, exercise therapy, sensory stimulation, acupuncture, hyperbaric oxygen chamber, transcranial magnetic stimulation, transcranial direct current stimulation, and other approaches are currently used in clinical practice for the treatment of PVS.

Although there are many methods for promoting wakefulness, the mechanism for awakening remains unclear, and efficacy evaluation is not yet standardized. Herein, we report a case of a patient with PVS following brain injury who received conventional rehabilitation therapy combined with sensitive sensory stimulation and awakening therapy and was monitored by long-term video electroencephalogram (EEG), EEG, and evoked potential.

Case Report

Ethics statement

The study participant voluntarily agreed to participate in the study and provided written informed consent prior to enrollment. This study was approved by the Ethics Committee of Shanghai Tongren Hospital, Shanghai Jiao Tong University School of Medicine (approval No. 2015-009-01). All procedures involving human participants were performed in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Patient information

The patient in this study was 36 years old, of Han nationality, and was previously in healthy physical condition. His family denied any history of chronic diseases such as hypertension, diabetes, and coronary heart disease, as well as infectious diseases such as viral hepatitis and tuberculosis. The patient had no history of food or drug allergy and no history of other surgery and trauma.

Timeline

On March 1, 2014, the patient sustained an accidental blunt traumatic head injury from impact by a heavy object, resulting in immediate loss of consciousness, right ear bleeding without coagulation, and urinary incontinence. The patient was immediately admitted to the emergency department. Under general anesthesia, the patient underwent decompressive craniotomy with the evacuation of an epidural hematoma on the right side of the temporal lobe in addition to intracranial pressure probe implantation. The patient entered a deep coma after surgery and was given treatments such as anti-inflammatory medication, hemostasis, brain training and dehydration, intermittent lumbar drainage, and tracheotomy. On March 21, the patient exhibited occasional automatic blinking. On May 11, the tracheal tube was removed, and tracheal sealing was successful. On May 15, the patient’s condition was stable, and the patient was then transferred to the rehabilitation department.

Clinical findings and assessments

The patient was in a state of inconsistent awareness at the time of admission to the rehabilitation department, and the patient blinked spontaneously with no light avoidance and observed visual evasion and tracking. The patient did not respond to the doctor’s instructions at the time of admission and was unable to follow movements. No spontaneous activity in the limbs was observed. The patient received a nasal feeding diet via an indwelling catheter, and also presented with urinary incontinence. Physical examination revealed an altered level of consciousness, unresponsiveness to external stimuli, lack of cooperation during examination, a right skull defect, collapse of the decompression window, and bilateral pupils of varying sizes, with left and right pupil diameters of ~3.5 mm and 1.5 mm, respectively. The patient was sensitive to light but showed no active limb movement under stimulation, and had a low muscle tone bilaterally, right lower limb swelling, weak right foot arterial pulsation, bilateral positive Babinski sign, positive Chaddock sign, a neck soft, and negative Klinefelter’s sign. The patient had a Glasgow score of 9 points. The following diagnosis was made: severe open TBI, cerebral hernia, traumatic subarachnoid hemorrhage, contusive brain injury, primary brain stem injury, skull base fracture, cerebrospinal fluid ear leakage, skull fracture, orbital wall fracture, scalp hematoma, and right lower extremity venous thrombosis.

The initial treatment after admission was as follows: 1) Neurotrophic factors supporting nerve repair (methylcobalamin tablets (Eisai (China) Pharmaceutical Co., Ltd., Shanghai, China), 0.5 mg, three times a day, per os), waking brain resuscitation (Xingnaojing injection (Henan Tiandi Pharmaceutical Co. Ltd., Kaifeng, China), 20 mL, twice a day, intravenously guttae), prevention of epilepsy (compound sodium valproate sustained release tablets (Chongqing Xindong Biotechnology Co., Ltd., Chongqing, China), 0.5 g, once a day, per os), phlegm reduction (ambroxol hydrochloride tablets (Shanghai Boehringer Ingelheim Pharmaceutical Co. Ltd., Shanghai, China), 30 mg, three times a day, per os), gastric mucosa protection (omeprazole magnesium enteric-coated tablets (Xinhe Yuansheng Pharmaceutical Co., Ltd., Gushi, China), 20 mg, once a day, per os); 2) Placement of the limb in a good position, mainly to inhibit the occurrence of spasm patterns. The position of the affected side, uninjured side, and supine position was adjusted every 2 hours; 3) Physical therapy, mainly included releasing the shoulder joint, passive scapula movement, inducing upper limb separation movement, improving abnormal muscle tension of the upper limb, and improving upper limb movement control (60 minutes once a day, 5 days per week); 3) Acupuncture, abdominal massage to improve stool and bladder function, mainly at Zhongwan (RN12), Xiawan (RN10), Qihai (CV6), and Guanyuan (RN4) for 20 minutes, once a day, 5 days per week. Acupuncture mainly on Shuigou (GV26), Baihui (DU20), Hegu (LI4), Neiguan (PC6), Zusanli (ST36), Taichong (LR3), and Yongquan (KI1) for 20 minutes once a day, 5 days per week; 4) Hyperbaric oxygen therapy for 2 hours, once a day, 5 days per week; 5) Use of the Disorder of Consciousness Scale (DOCS) to evaluate the olfactory, auditory, visual, proprioceptive, tactile, and swallowing functions in the patient semimonthly. Patients with no response were rated as 0 points, generalized response was 1 point, localized response was 2 points, screening of sensitive stimuli (2 points); 6) Patting of the back, applied air pressure, and other approaches to prevent decubitus ulcer, venous thrombosis, and other complications. In the course of the disease, Glasgow Coma Scale, DOCS, Barthel Index, video long-range EEG monitoring, EEG, and evoked potentials were evaluated for a 5-month follow-up period [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]. After 5 months of treatment, the patient regained consciousness with improved bladder and bowel function. Electroencephalogram indicated that the brain function was significantly improved. Auditory evoked potentials and somatosensory evoked potentials suggested that the sensation conduction pathways had improved significantly. Sensitive sensory stimulation in combination with routine rehabilitation treatment can effectively cause the regain of consciousness in patients with persistent vegetative state following TBI and improve activities of daily living and the function of the sensation conduction pathways.

Table 1: Glasgow Coma Scale scores of patients with persistent vegetative state following traumatic brain injury

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Table 2: Disorder of Consciousness Scale scores of patients with persistent vegetative state following traumatic brain injury

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Table 3: Barthel index of patients with persistent vegetative state following traumatic brain injury

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Table 4: Long-term video electroencephalogram monitoring in patients with persistent vegetative state following traumatic brain injury

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Table 5: EEG changes in patients with persistent vegetative state following traumatic brain injury

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Table 6: Evoked potentials change in patients with persistent vegetative state following traumatic brain injury

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Discussion

Jennett and Plum (1972) first defined PVS as unconscious awakening. The diagnostic criteria for vegetative state are: 1) No self and environmental awareness, inability to interact with others; 2) No sustained, repetitive, purposeful, or voluntary response to visual, auditory, tactile, or noxious stimuli; 3) Inability to understand or express speech; 4) A sleep-wake cycle with intermittent awakening; 5) Well preserved hypothalamic and brainstem autonomic nervous function, and medication and care is sufficient for the patient to survive; 6) Rectal and bladder dysfunction; 7) Cranial nerve reflexes (pupil, head, and eye reflexes, cornea, vestibular-ocular function, and vomiting) and spinal cord reflexes are preserved in different degrees. Recovery of consciousness in patients with PVS 12 months after trauma and in patients with PVS longer than 3 months after non-traumatic disorders is extremely rare. Giacino et al. (2002) proposed the concept of minimally conscious state, that is, inconsistent but discernible behavior that can be distinguished from coma or vegetative state.

Sensory stimulation of wakefulness was first applied in the early 1950s, and refers to the use of visual, olfactory, auditory, gustatory, and tactile stimuli to elicit meaningful behavioral responses (Dos Santos et al., 2019). A possible mechanism for such responses is that sensory stimulation can promote dendritic growth and strengthen synaptic connections. Extrinsic stimulation can also prevent patients with PVS from experiencing sensory deprivation, improve neural repair, and increase brain plasticity. In addition, with the regeneration of collateral axons in the central nervous system, patients with PVS who receive intense and frequent sensory stimuli will form new sensory conduction pathways, and the brain’s reticular system will receive feedback and respond to stimuli (Sarracino et al., 2020). In this patient’s sensory stimulation treatment, the following three aspects were followed: 1) Standardized treatment: The environment was kept quiet, with only one therapist leading a conversation with the patient and preventing habitual reactions. Each stimulus lasted approximately 10–15 minutes, with 5 minutes rest after each stimulus; 2) Correct body position: When visually stimulated, the headboard of the bed was elevated high enough to provide normal visual direction, which can facilitate visual tracking in the patient; 3) Enhanced sensitive stimulation: DOCS were evaluated semimonthly, and the types of stimuli that triggered local reactions were selected to enhance stimulation. In addition, drug therapy was administered to improve cerebral blood circulation, improve blood nutrient and oxygen supply to the brain, and promote neurological function recovery. Routine rehabilitation treatment was administered to prevent muscle atrophy, maintain joint mobility, and improve physical activity.

Current clinical evaluation of the treatment efficacy of patients with PVS mainly includes physical indicators (Poza et al., 2013), scale evaluation (American Congress of Rehabilitation Medicine et al., 2010), EEG (O’Donnell et al., 2021), evoked potentials, functional magnetic resonance (Jang et al., 2021), and positron emission tomography (Picelli et al., 2015). The study presented here used patient functional scoring scales, video long-range EEG monitoring, EEG, and evoked potentials for comprehensive, objective, quantitative assessment. The Glasgow Coma Scale score increased from 9 points before treatment to 11 points after treatment, with 1 point for exercise and language respectively. The DOCS score increased from 22 to 54 points. The Barthel index increased from 0 to 15 points, mainly in the control of urine and stool function. Long-term video EEG monitoring and EEG suggested that the patient had a sleep cycle, and that the brain function had significantly improved. Somatosensory evoked potentials are an objective tool that reflects the integrity of somatosensory pathways (Meyer et al., 2014). Damage to the central nervous system often causes adjacent sensory and motor pathways to be damaged simultaneously. Therefore, it is suggested that somatosensory evoked potentials can effectively assess the prognosis of limb function following central nervous system injury (Rollnik, 2015; Hwang et al., 2016). In this study, the patient’s somatosensory evoked potential waveforms indicated improvement. Sensory and motor conduction functions were also improved. Auditory evoked potentials have an important reference value for the prognosis and outcome of unconsciousness and coma (Wang and Wang, 2016). The left ear auditory evoked potential waveform changed from abnormal to almost normal, which also indicated the efficacy in promoting PVS wakefulness.

Therefore, with the identification and use of specific types of sensitive sensory stimuli in patients with PVS who have sustained a brain injury, such sensory stimulation combined with conventional rehabilitation and drug therapy can effectively waken patients with PVS and improve their sensorimotor function and daily living ability. However, the selection of sensitive sensory stimuli and the type, intensity, time, and frequency of stimuli needs further study to provide a broader range of application of sensitive sensory stimuli arousal therapy.

The case was a clinically successful one. Due to the limitations in sample size and equipment, we were unable to provide our therapies to all the patients with PVS. Another limitation is the lack of long-term follow-up such as 1 or 2 years later because such a long-term evaluation is not allowed, which may be prone to biases. Future studies will be established to address and resolve these questions.[18]

Author contributions

Conception and design: YL, HWM; data collection, assembly, analysis and interpretation: HWM. Both authors conceive conception and design the work, wrote the manuscript and approved the final manuscript.

Conflicts of interest

No potential conflict of interest was reported by the authors.

Open access statement

This is an open access journal, and articles are distributed under the terms of the Creative Commons AttributionNonCommercial-ShareAlike 4.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as appropriate credit is given and the new creations are licensed under the identical terms.

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