Abstract
BACKGROUND:
There are several gaps in the literature related to the prognosis and care of children who have experienced a brain injury then develop paroxysmal sympathetic hyperactivity (PSH).
OBJECTIVE
: The objective of the present study was to explore the characteristics and prognosis of children who have experienced severe brain injury and developed PSH.
METHODOLOGY:
A secondary analysis was conducted using an established clinical dataset of children
who had experienced severe brain injury and were admitted to an academic children’s
rehabilitation center (
RESULTS:
Those children with PSH had a significantly longer acute care length of stay
(
IMPLICATIONS:
The findings from the present study reveal factors regarding the elusive phenomenon of PSH among children.
Introduction
Pediatric brain injury can cause devastating injuries that can last throughout a lifespan. The Center for Disease Control and Prevention has declared brain injury a public health emergency in the United States with an estimated 1.7 million traumatic brain injuries (TBIs) annually. An injury to the brain may be traumatic or non-traumatic. Falls, motor vehicle accidents, bike accidents, gunshot wounds, sports injuries, assaults, and military or workplace injuries can cause TBIs, while non-traumatic injuries can be caused by stroke, seizures, tumor, infection, hypoxia, or toxic exposures [1]. The leading causes of brain injuries in children vary by specific age groups [1]. While the majority of brain injuries are classified as mild, 25% are considered moderate to severe, resulting in significant cognitive and motor impairment [1].
Paroxysmal sympathetic hyperactivity (PSH) is a confounding phenomenon that occurs after severe brain injury. PSH presents clinically as a cluster of symptoms that includes hyperthermia, hypertension, tachycardia, tachypnea, diaphoresis, and/or dystonia [2, 3, 4, 5, 6, 7]. Different nomenclatures have been used to describe this phenomenon, however, an international expert consensus group has endorsed the term PSH [7].
In the adult literature, this symptom cluster following severe brain injury has been associated with prolonged hospitalizations and poorer cognitive and motor function [2, 5, 8, 9, 10]. Developing evidence in pediatric patients points to similarly dismal outcomes [6, 7]. Only a few studies have explored PSH in children following brain injury; therefore, outcomes for children with PSH are largely unknown, leaving a gap in the literature [6, 7, 11, 12]. Further investigation is needed related to PSH and the association of these symptoms with outcomes in children with brain injury. Additionally, very little is known about the ability to transition to rehabilitation for those that exhibit PSH.
The major objective of the present study was to explore the characteristics and prognosis of children who have experienced severe brain injury and develop PSH. The results of the present study will provide clarity regarding the relationship between PSH prognoses in children following severe brain injury. The present study used a secondary analysis of an established clinical dataset of children who had experienced a severe brain injury and were admitted to an academic children’s hospital rehabilitation center. The specific aims were as follows: (1) to evaluate the differences in demographic and injury-related variables between children with severe brain injury with and without PSH, (2) to determine the relationship between transition to rehabilitation with and without PSH, and (3) to evaluate the influence of PSH as a predictor of lower cognitive function, poorer motor function, and longer hospital length of stay.
Methodology
Research design
The present study used a retrospective, secondary analysis of a clinically established dataset of children who had experienced a severe brain injury i.e., (had not regained functional arousal, awareness, and communication). Children were enrolled in the dataset consecutively. The clinical dataset (1998–2012) was established at the University of Virginia Children’s Hospital Kluge Children’s Rehabilitation Center (KCRC) for the purpose of documenting and monitoring clinical outcomes after a child had experienced a severe brain injury.
Setting and subjects
The KCRC was a referral facility providing inpatient acute care and rehabilitation services to children who experienced brain injuries in Central Virginia from 1957–2011. The dataset included 40 clinical variables from 83 children. The sample of children ranged in age from 2 months to 21 years. Traumatic and non-traumatic etiologies, males and females, and all races were included.
Children that experienced severe brain injury and had not regained consciousness were admitted to KCRC for acute care service following transition from an intensive care unit. The child needed to be deemed medically stable (i.e., no acute neurosurgical issues, tolerating enteral feeds via feeding tube, tracheostomy in place if needed) to be accepted in acute care. This transition may be considered equivalent to transfer to a general (non-ICU) medical unit. The primary goals at this level of care at KCRC included simplifying medication regimens, symptom management, and managing comorbid or iatrogenic factors that could hinder emergence. Once addressed, some children spontaneously recovered functional skills and were able to transition to rehabilitation status pending insurance approval. During the rehabilitation stay, the child received three hours of therapies per day (combination of physical, occupational and speech therapy based on individual needs). If a child did not regain functional skills and the acute care medical goals were achieved, the child was discharged from KCRC without transitioning to rehabilitation.
Data collection protocol
The dataset was established and maintained electronically from a retrospective review of medical records after the child was discharged from KCRC. The acute hospitalization and rehabilitation courses at KCRC of patients were not altered in any way. The individuals who entered the data and performed the reviews did not discuss the variables with the medical providers or staff taking care of the children. This minimized bias in data collection. The presence of PSH was determined by clinical diagnosis and/or the presence of medication treatment and documentation by the attending medical provider at KCRC in the medical record. The University of Virginia Institutional Review Board approved the establishment and management of the dataset, as well as the statistical analysis plan for the present study.
Variables and measures
For Aim 1, demographic characteristics of the children included age, age
group (
For Aims 2 and 3, the dependent variables of interest included motor and cognitive function, length of hospitalization at KCRC, and transition to rehabilitation. These variables have been defined in the literature as predictors of recovery trajectory following brain injury in children [6, 7]. The instruments used to assess cognitive (Rancho Los Amigos Scale, Western Neuro Sensory Scale Profile) and motor (Functional Independence Measure for Children) function have demonstrated appropriate psychometric properties [15, 16, 17, 18, 19].
The Rancho Los Amigos (RLA) Scale is an observational, descriptive scale of the eight stages of cognitive function following brain injury [16]. A higher stage indicates better function. For the present study, this scale was documented in the medical record by an experienced pediatric nurse practitioner and/or an attending medical provider and was based on their clinical expertise as part of routine assessments of children with brain injuries. The RLA was documented on admission and discharge from KCRC.
The Functional Independence Measure for Children (WeeFIM) is an instrument used to measure the need for assistance and to document the severity of disability in children. A higher score indicates better function. Initially, the WeeFIM was limited to children 6 months to 7 years old; however, the instrument has been standardized for use in adolescents. For the present study, certified therapists administered and documented the results in the medical record as part of routine assessments of children with brain injuries only if a child successfully transitioned to rehabilitation and upon discharge from KCRC. In addition, children under 6 months of age were excluded from the WeeFIM analysis because the instrument is not deemed reliable or valid in that age group [17, 18, 19].
The Western Neuro Sensory Scale Profile (WNSSP) scale is used to monitor and predict small changes in individuals who have not regained consciousness [15]. A higher score indicates better function. In the present study, the WNSSP was administered and documented in the medical record by a credentialed speech language pathologist who administered the instrument as part of routine assessments of children with severe brain injuries and who documented upon admission and discharge from KCRC.
Statistical analysis
Demographic characteristics by PSH status
Demographic characteristics by PSH status
The computer software package nQuery Advisor 7.0 (Statistical Solutions
Ltd., Dublin, Ireland) was used to conduct a power analysis using several regression
models prior to the initiation of the current analyses. Multiple regression was used for
the continuous dependent variables (motor and cognitive function). For a multiple
regression model that already includes 3 covariates (age, gender, injury type) with
squared multiple correlation
Data were analyzed using SPSS version 22. Aim 1: Descriptive statistics
(means and standard deviations or frequencies and proportions) were computed for the
demographic variables and by the presence or absence of PSH (any PSH [yes/no]). Bivariate
tests (chi-square for categorical variables,
Aim 2: Logistic regression was used to estimate the effects of PSH on
transition to rehabilitation (yes/no), while taking into account age, gender, and etiology
of brain injury. Aim 3: Multiple regression was used to estimate the effect of PSH on the
continuous outcomes of motor (WeeFIM) and cognitive function (RLA, WNSSP) and length of
stay at KCRC (in acute care, in rehabilitation, and total), while taking into account age,
sex, and etiology of brain injury. Data were transformed using LOG10 when assumptions were
not achieved for the length of stay variables. Two-tailed tests with
Demographic characteristics of the total sample between those with and without
PSH are reported in Table 1. There was a significant
difference in spasticity treatment for those children exhibiting PSH compared with those who
did not (
Characteristics of children who did and did not transition to rehabilitation are
reported in Table 2. There was a significant
difference in age (
Characteristics of children who did and did not transition to rehabilitation
Characteristics of children who did and did not transition to rehabilitation
Clinical outcomes by PSH status are reported in Table 3. Sixty-five percent of the sample transitioned to rehabilitation
with a mean admission total WeeFIM score of 27.80
Clinical outcomes by PSH status
There was a significant difference in admission WNSSP score by PSH status
(
There were no significant differences between admission and discharge WeeFIM
self-care or mobility scores by PSH status (Table 3).
After controlling for age and etiology of injury, PSH was not a significant predictor of
admission WeeFIM self-care scores (coeff
There was a significant difference in acute care length of stay
(
Those children who exhibited PSH had an increased frequency of receiving management for spasticity, a condition and form of hypertonia characterized by muscle tightness and stiffness.
Given that motor overactivity and dystonia are both recognized as features of PSH, it is reasonable to suspect that individuals with PSH would exhibit abnormal muscle tone and require treatment. No other differences in demographic or injury-related variables by PSH status were noted.
The children who transitioned to rehabilitation exhibited different characteristics compared with those who did not. The group who did not transition to rehabilitation was younger (mean age 10.06) compared with those who did (mean age 18.03). There was a significant difference between etiology of injury and rehabilitation groups. Eighty-five percent of those who transitioned to rehabilitation had suffered traumatic brain injuries. In the group who failed to transition, 34.5% experienced an acquired or non-traumatic brain injury. It has been speculated in the literature that children who experience acquired brain injuries have a poorer recovery trajectory then those with traumatic injuries [21]. Another difference between groups was among those who received low response medication to promote arousal and awareness. Those who received low response medication had an increased frequency to transition to rehabilitation compared with those who did not receive low response medication. It is important to acknowledge that in 2006 the KCRC published the results of a randomized control trial that used dopamine-agonist medications to promote arousal and supported the use of low response medications in children following severe brain injury [22]. Following that study, there was a shift in practice and the use of low response medications became standard practice.
PSH was not a significant predictor in cognitive and motor function after controlling for age and etiology of injury in this sample. Additionally, PSH was not associated with transition to rehabilitation after controlling for age and etiology of injury. The lack of differences could be related to the significant differences between acute and total lengths of stay at the rehabilitation center. Those with PSH had significantly longer acute care and total lengths of stay at KCRC, which could have allowed for continued recovery of function, thus allowing for transition to rehabilitation at a later date. The longer acute length of stay at KCRC could have been attributed to the presence of PSH. Children with PSH may have needed additional days in acute care to manage their symptoms before transitioning to rehabilitation. The present study demonstrates that although PSH is a complicated phenomenon following severe brain injury in children, motor and cognitive improvements can be achieved. Children who experienced PSH following a severe brain injury do make progress; however, it takes time and may require a longer acute care course prior to transition to rehabilitation.
There are several limitations of the present secondary analysis that need to be acknowledged given the retrospective design. All variables included in the dataset were obtained from retrospective chart review after the child was discharged from KCRC. The instruments collected were administered for clinical purposes and were not part of a rigorous clinical trial. The existing clinical dataset did not include some variables of interest (i.e., data related to costs, ethnicity, and readmission). The date of injury was not included, and thus days post injury were unable to be calculated. Additionally, the race demographic variable was not self-reported. The length of stay data was also only from a single center and did not include hospitalization prior to admission to KCRC.
PSH was based on clinical assessment, judgment, and documentation. This method of determining PSH has been used in other studies [6, 7]. However, there are several limitations to this method of classifying PSH. First, this method could underestimate prevalence because recognition, identification, management, and treatment of PSH can vary based on the provider. According to the literature, the prevalence of PSH in adults is reported between 8–33% following brain injury [8, 9, 10, 23]. Both Kirk and colleagues [6] and Krach and colleagues [7] have reported the pediatric prevalence of PSH as 13–14%, although there have been no prospective pediatric studies to document the incidence of PSH [6, 7]. The present study reported a higher prevalence (47%) following severe brain injury in children. The prevalence may be higher then previously reported because the children in our sample experienced severe brain injuries requiring transfer to KCRC as opposed to children who initially have a low GCS and recover quickly. Unfortunately, descriptive information regarding PSH was not captured in the dataset based on the categorization, thus specific characteristics regarding prescence and timing were not available.
Conclusion
Children who experience severe brain injuries can have life-long disabilities. The present study addresses gaps in the literature by focusing on a sample of children with severe brain injury who had not regained consciousness and required maximum care. Results of the present study have revealed factors regarding the elusive phenomenon of PSH. In this sample, PSH following pediatric brain injury was not a significant predictor of poor motor or cognitive function when compared with children with a severe brain injury in the absence of PSH after controlling for age and etiology of brain injury. It was noted that there was a significant difference based on acute and total length of stay between PSH and those that did not demonstrate PSH. However, there was not a difference in rehabilitation length of stay. Recovery for children that experience PSH is at a different trajectory. Further research on PSH and associated outcomes in children with brain injury is needed to improve the care and quality of life of this vulnerable population of children, as well as their families and communities.
Footnotes
Conflict of interest
No actual or potential conflicts of interest. No external or intramural funding was received.
