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Article

Neurocognitive Sequelae and Rehabilitation after Subarachnoid Hemorrhage: Optimizing Outcomes

by
Divine C. Nwafor
1,2,
Brandon D. Kirby
1,2,†,
Jacob D. Ralston
1,†,
Mark A. Colantonio
1,
Elochukwu Ibekwe
3 and
Brandon Lucke-Wold
4,*
1
Department of Neuroscience, West Virginia University Health Science Center, Morgantown, WV 26506, USA
2
Rockefeller Neuroscience Institute, West Virginia University, Morgantown, WV 26506, USA
3
Department of Neurology and Neurocritical Care, The Ohio State University, Columbus, OH 43210, USA
4
Department of Neurosurgery, University of Florida, Gainesville, FL 32611, USA
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
J. Vasc. Dis. 2023, 2(2), 197-211; https://doi.org/10.3390/jvd2020014
Submission received: 12 January 2023 / Revised: 14 February 2023 / Accepted: 8 March 2023 / Published: 1 April 2023
(This article belongs to the Section Neurovascular Diseases)
Browse Figure
Review Reports Versions Notes

Abstract

:
Subarachnoid hemorrhage (SAH) is a medical emergency that requires immediate intervention. The etiology varies between cases; however, rupture of an intracranial aneurysm accounts for 80% of medical emergencies. Early intervention and treatment are essential to prevent long-term complications. Over the years, treatment of SAH has drastically improved, which is responsible for the rapid rise in SAH survivors. Post-SAH, a significant number of patients exhibit impairments in memory and executive function and report high rates of depression and anxiety that ultimately affect daily living, return to work, and quality of life. Given the rise in SAH survivors, rehabilitation post-SAH to optimize patient outcomes becomes crucial. The review addresses the current rehabilitative strategies to combat the neurocognitive and behavioral issues that may arise following SAH.

1. Introduction

Subarachnoid hemorrhage (SAH) is a devastating condition with high mortality and morbidity rates and is often accompanied by significant physical, behavioral, and neurocognitive comorbidities [1]. These comorbidities present acutely (within three months) and persist long-term (up to two years) post-SAH [2,3]. The behavioral and neurocognitive sequelae associated with SAH include psychological distress affecting mood and anxiety, post-traumatic stress disorder (PTSD), social dependence, fatigue, and alterations in sexual function [3,4].
Regardless of SAH severity, a significant number of SAH patients develop neurocognitive and behavioral psychosocial issues due to several mechanisms that may include: organic brain injury secondary to vascular disruption; the unmasking of underlying neuropsychiatric conditions; development of PTSD following hospitalization; and associated life stressors (e.g., unemployment, etc.) [5,6]. The present review discusses the neuropsychiatric and cognitive sequelae post-SAH. Furthermore, we highlight current evidence-based rehabilitative strategies to combat the neurocognitive and behavioral issues that may arise following SAH in the acute and chronic stages.

2. Neuropsychiatric and Neurocognitive Sequelae Following SAH

2.1. Depression

Depression has been reported after SAH and appears to persist [7]. The frequency of depression following SAH is variable and depends on the timing of assessment following the SAH ictus. A recent meta-analysis by Tang et al. showed that the overall pooled frequency of depression was 26.3% post-SAH. Furthermore, the progression of depression from months to years in the SAH ictus also depended on the assessment tools utilized [8]. In another study, depressed mood occurred in 47% of patients during the first year of recovery post-SAH; notably, in the same study, non-Caucasian ethnicity was a risk factor for developing depression post-SAH [9]. Other premorbid conditions, including a prior history of mood disorders, tobacco use, alcohol use disorder, illicit drug use, chronic obstructive pulmonary disease, and non-English fluency, have been shown to increase the risk of depression following SAH [7,8]. Additionally, patients with posterior circulation aneurysm rupture have been shown to have significantly more problems with depression [10].
Depression significantly affects the patient’s quality of life, employment, and functional outcomes following SAH [9,11]. The mechanism for depression post-SAH remains unclear; some studies have proposed a link between low basal cortisol levels and depression post-SAH [12,13]. Given this association, future studies are warranted to investigate the contributions of the hypothalamic-pituitary-adrenal (HPA) axis in post-SAH-associated depression.
Despite the prevalence of depression post-SAH, there is a paucity of data on the treatment of post-SAH depression. In the general population, selective serotonin receptor inhibitors (SSRIs) are the first-line antidepressant drugs used to manage depression [14]. Given the risk of intracerebral hemorrhage (ICH) with SSRIs within the first month of use, the optimal initiation of antidepressants while exploring other pharmacological and multimodal treatment strategies needs to be studied in SAH survivors [15]. Such options for multimodal therapy may include light and music therapy, motivational interviewing, transcranial magnetic stimulation, ecosystem-focused therapy, etc.

2.2. Anxiety

Given the strong association between anxiety and depression, assessing anxiety in patients post-SAH is paramount. Similar to depression, the prevalence of anxiety post-SAH is dependent on the study tools utilized and the timing of the assessment. For instance, Barlet et al. showed a pooled anxiety prevalence of 32.2%, 19.2%, 40.5%, and 47.6% prevalence at 3, 6, 12, and 24 months, respectively, post-SAH. Using the State Trial Anxiety Inventory method, the overall increased anxiety burden post-SAH showed statistically increased anxiety symptoms of 39%, 41%, and 54% at 3 months, 1 year, and >2 years follow-up, respectively, post-SAH [16]. Passive coping strategies, unemployment at 6 months, and a prior history of a psychiatric disorder were associated with an increased risk of an anxiety disorder post-SAH [11]. Additionally, patients with posterior circulation aneurysm rupture have been shown to have significantly more problems with anxiety [10]. Further research is needed to delineate the brain circuits and neurochemical factors that perpetuate anxiety post-SAH.

2.3. PTSD

PTSD post-SAH is prevalent and associated with poor quality of life despite relatively good clinical outcomes [17,18,19]. The prevalence of PTSD following SAH ranges from 18–37% [17,18]. The variability in prevalence arises from differences in the assessment tools utilized and the timing of assessment. Importantly, significant others/caregivers (e.g., spouses, etc.) of patients who survived SAH have been shown to have increased symptomatology of PTSD. This finding is important given that PTSD in this subgroup could interfere with effectively administering care to SAH patients [20,21].
While the underlying mechanism for PTSD following SAH remains unclear, some studies have suggested that PTSD post-SAH may result from the patient’s adjustment to the experience of having had a SAH and the fear of recurrence [19,22,23]. Risk factors for PTSD post-SAH are similar to those for depression and anxiety. Notably, patients with a history of psychiatric disorders are more at risk of developing PTSD following SAH [17].

2.4. Sexual Dysfunction

Brain injury can affect the way patients express their sexuality. Many patients following brain injury have reported reduced sexual drive, reduced arousal, impotence, or increased compulsive sexual behaviors [24]. Sexual dysfunction as it relates to SAH is understudied; several studies have shown that both men and women report sexual dysfunction and dissatisfaction following stroke [25,26,27]. These findings become relevant when caring for patients post-SAH, since SAH can cause stroke secondary to hemorrhagic ischemia [28]. In another study, 9 of 19 women (47%) reported having sexual dysfunction according to the female sexual function index (FSFI) following an aneurysmal SAH (aSAH). Interestingly, all 19 of the women reported having hypoactive sexual desire disorder. The authors also noted that 7 of 14 men had erectile dysfunction using the International Index of Erectile Function (IIEF) [4]. While the exact mechanisms responsible for sexual dysfunction post-SAH remain unclear, some studies have suggested that hypothalamo-pituitary dysfunction may contribute to impaired sexual function post-SAH [29,30].

2.5. Cognitive Dysfunction

Cognitive dysfunction is a common issue following SAH due to the diffuse brain injury that occurs during the initial insult. Various cognitive domains may be affected, including memory, language, spatial processing, and executive function, even if patients appear relatively clinically normal at discharge [31]. Furthermore, many of these complications are long-term and continue to affect patients in the months following discharge, appearing to have a significant impact on quality of life and return to work [32,33,34]. In a retrospective study, 94.6% of patients evaluated 3 months post-SAH had at least one cognitive deficit, the most common being memory [35]. Despite the high probability of cognitive deficits in the SAH population, these complications go underreported [36].

3. Rehabilitation after Subarachnoid Hemorrhage in the Acute Setting

The diagnosis of SAH from a ruptured aneurysm or traumatic cause is typically established in the emergency setting. Once this is established, care is transitioned to a neurosurgical team, if necessary and not contraindicated, and then to a neurocritical care unit (neuro ICU). Patients may present with various neurological symptoms, but the most common is a severe headache refractory to home treatment. While only 1% of headaches presenting in the emergency department (ED) are attributed to subarachnoid hemorrhage, the mortality rate of SAH may be as high as 65%. Early diagnosis in the ED and prompt patient stabilization are vital to reducing mortality [37]. This section briefly discusses the management of SAH in the acute setting and rehabilitative strategies that improve patient outcomes.

3.1. Fluid and Electrolyte Management

An initial primary goal in the neuro ICU is proper fluid management to prevent secondary cerebral injury due to poor cerebral perfusion and inadequate cerebral oxygenation. Volumetric status is typically aimed at euvolemia with constant hemodynamic monitoring, such as central venous pressure, pulmonary wedge pressure, and fluid balance [38]. Fluid status is generally achieved via a mean intake of 3–4 L per day of crystalloids [39]; however, the choice of crystalloids is currently being evaluated in a current clinical trial (NCT04043598). Current and past clinical trials have also evaluated more aggressive fluid strategies such as hypervolemia, steroid-based therapies as opposed to crystalloids, and others; however, there has been no evidence to suggest any benefit over the current fluid management strategies [39]. Some studies suggest that hypervolemic goals increase the risk of complications and result in poorer outcomes [40].
Fluid status is also important in preventing other post-SAH metabolic-related complications such as hyponatremia, anemia, and hypo- or hyperglycemia [41,42,43]. Hyponatremia is an especially common complication and can lead to further adverse events such as delayed cerebral ischemia and symptomatic vasospasm [40]. The current guidelines for treating hyponatremia recommend using hypertonic saline and/or steroid-based therapies to correct the electrolyte imbalance and avoid free water and fluid restriction [40]. However, care must be taken to prevent rapid correction of the sodium imbalance so as to prevent central pontine myelinolysis [44]. Clinical trials have evaluated the use of ADH receptor antagonists, such as conivaptan, but have been unsuccessful due to adverse effects from rapid imbalance correction [45]. The guidelines for treating anemia and hypoglycemia are well established and involve the use of packed red blood cells and glucose, respectively [40].

3.2. Nutritional Rehabilitation

Nutritional goals have also proved vital in the acute setting. The international guidelines for nutrition in the critically ill are typically followed, as there are no defined guidelines for SAH at the time of this review [46,47]. These current guidelines suggest that an oral diet should be maintained if the patient is able to eat and cover at least 70% of their nutritional needs [46]. If the patient is unable to eat, enteral nutrition (EN) or parenteral nutrition (PN) should be started promptly. EN is typically preferred in SAH patients, but many studies suggest this route does not meet the nutritional requirements and may increase the risk of adverse events [48,49].
Further studies have recommended the initiation of supplemental PN if EN cannot meet the caloric requirements needed to reduce mortality in critically ill patients [50]. Higher protein intake has also been shown to decrease mortality and lead to favorable outcomes [51]. Based on the current data, nutrition should be addressed early through the use of both EN and PN to achieve adequate caloric and protein intake to reduce complications and mortality.

3.3. Early Mobilization and Cognitive Rehabilitation

Early mobilization has been addressed in the acute setting post-SAH. A prospective, interventional study compared SAH patients who received standard mobilization therapy with those who received early mobilization therapy. Karic et al. found that early mobilization did not increase complications, and other adverse events, such as thromboembolic events or even death, were similar between the groups. Interestingly, the risk of severe vasospasm decreased by 30% in the early rehabilitation group [52]. A retrospective study compared early and late mobilization groups and found that patients in the early mobilization group had earlier discharges to home with better functional status at discharge [53]. Lastly, a randomized clinical trial (RCT) compared early mobilization within 24 h to the current standard of care for acute ischemic or hemorrhagic stroke and found fewer patients in the early mobilization group had favorable outcomes at 3 months [54]. Based on the current data, early mobilization and rehabilitation in SAH patients may be feasible, but more studies primarily focusing on SAH patients are needed to determine the effect on outcomes precisely.
Early mobilization may also influence the improvement of cognitive function following SAH. Considering the impact cognitive deficits have on the quality of life following SAH, very little information exists on the benefit of focused cognitive rehab in the acute setting aside from the cognitive benefits shown as a result of early mobilization [36]. Furthermore, the timing of when to initiate early cognitive rehabilitation should also be considered and studied.
Neuropsychological tests may be used to determine the specific deficits, and the recommendation for which tests are ideal varies between studies [31,55]. Neuropsychological tests routinely used in the acute setting following SAH include the modified Rankin Scale, the Montreal Cognitive Assessment, and the MMSE; however, these tests poorly predict minor cognitive deficits. Specific neuropsychological tests, such as the CVLT-II, the Ray Osterich Complex Figure Tests, etc., for memory, may provide more sensitivity to better understand the extent of cognitive deficits and the cognitive domains affected, such as memory, learning, language, spatial awareness, etc. [31].
Once specific cognitive deficits in SAH patients in the acute setting are determined via neurocognitive testing, decisions on cognitive rehabilitation should be promptly initiated. Initiating cognitive rehabilitation too early or delaying it may hinder success and lead to suboptimal outcomes [56]. Rehabilitation should also be tailored to the specific deficit identified. Technology may be utilized as an option to initiate cognitive rehabilitation quickly. An RCT by Chen et al. recently studied the early initiation of cognitive rehabilitation using tablets and found the feasibility of using technology to help address cognitive issues in the acute setting. However, a limitation of this study was the small sample size of participants [57].
The current data utilizing cognitive rehabilitation in the acute setting is limited despite well-established cognitive deficits during this time frame. With the current trend of cognitive rehabilitation being initiated more in the sub-acute or chronic period, further studies into the initiation of cognitive rehabilitation in the acute setting and its effect on long-term quality of life are warranted.

3.4. Multidisciplinary Care

Considering the intensive care required and the wide range of complications that may arise in the acute setting of SAH, a multidisciplinary approach to care should be utilized. The primary teams involved in the initial diagnosis and treatment of SAH may include the ED teams, radiology/interventional radiology teams, neurosurgical teams, anesthesia teams, and neurocritical care teams. Treatment should be managed in a large facility with specialized neurological intensive care units to adequately provide the specialties needed for the immediate treatment of SAH. Following the early stages of care, several clinical specialties may also be consulted for optimal care [58]. Consulting specialties involved in fluid management and metabolic concerns in the acute setting may include cardiopulmonary specialists, endocrinologists, and nephrologists to address electrolyte and fluid abnormalities, as well as hematologists to address anemia concerns [59,60,61,62]. Dieticians and nutritional specialists may be involved in the nutritional aspects of care provided in the neuro ICU [63]. Several specialties may also be utilized for the mobilization and cognitive issues seen in SAH patients, including physical therapists, physiatrists, neuropsychologists and therapists, and psychiatrists [64,65,66]. While not all specialists listed may be directly involved, SAH patients benefit from a multidisciplinary approach and are more likely to be discharged home with fewer long-term complications [67,68,69].

4. Long-Term Rehabilitation Following Subarachnoid Hemorrhage

Advances in surgical techniques and medical management have led to a steady decrease in the mortality rate following SAH. Between 1980 and 2005, there was a 50% decrease in mortality rate and an absolute annual reduction of 0.9% in 30-day mortality post-SAH [70]. The improvement in SAH mortality has led to more survivors needing long-term treatment strategies to reintegrate into society. It is reported that one-third of these survivors have a reduced quality of life one year post-SAH ictus [71]. These data indicate a clear need for a multifaceted treatment plan following SAH to optimize long-term patient outcomes.

4.1. Long-Term Outcomes Following SAH

Following SAH, only 55% of patients regain functional independence, while 19% remain dependent, and 26% ultimately die [72]. Post-SAH, a high proportion of patients reported impairments in memory, executive function, and language that led to the deterioration of activities of daily living, return to work, quality of life, and instrumental activities of daily living [5]. One study showed that more than half of patients deemed to have had good neurological outcomes one year post-ictus experienced mild to moderate difficulties with reintegration 20 years post-SAH. With this, their general quality of life was not affected [73]. It was reported that 94.6% of patients with moderate to good physical recovery living at home post-SAH had at least one cognitive or emotional complaint that impeded day-to-day life [35]. Interviews with patients about discharge in a retrospective study showed that patients discharged directly from neuro ICUs felt abandoned, found it challenging to find the appropriate support, and were confused about rehabilitation. On the other hand, patients referred to a rehabilitation clinic stated that they felt supported and informed and described the process as organized. In general, these patients emphasized the need for multidisciplinary follow-ups, which were largely missing from their long-term treatment plans [74].

4.2. Determinants of Health Post-SAH

Managing the long-term ailments associated with SAH requires a functional understanding of the determinants associated with these ailments. Several studies utilize the health-related quality of life (HRQoL) to determine outcomes post-SAH [75]. Some factors that determine poor HRQoL in patients post-SAH include the severity of SAH, fatigue, mood problems, physical disability, cognitive complaints, passive coping, female gender, and neuroticism [16,75,76]. Additionally, it has been found that passive coping, living alone, unemployment, restrictions in leisure, and poor HRQoL are determinants of anxiety and depression in the long-term following SAH [16,77]. These determinants should be considered when designing long-term rehabilitation plans for SAH patients, as they mitigate many cognitive and behavioral issues post-SAH.
Returning to work is an essential milestone in long-term SAH recovery and is associated with good neurological outcomes [78]. Only one-third of all patients post-SAH return to work at full capacity [34,79]. A failure to return to work is associated with lower quality of life, depression, insomnia, panic, fatigue, and anxiety [79,80,81,82], whereas successfully returning to work is associated with higher satisfaction levels, self-care ability, and financial stability [79]. The factors that affect the success of returning to work are depression, state anxiety, and trait anxiety [83]. More recently, it has been argued that returning to driving should be used as a long-term milestone in SAH recovery. Lai et al. argue that return to work is not a reliable predictor of a patient’s status because of diverse determinants such as age, socioeconomic status, type of occupation, and complex psychosocial factors associated with returning to work. Additionally, return to driving is a more measurable outcome and is strongly associated with return to work, a positive neurological outcome, mobility, and return to daily living activities [78]. Notably, an equal amount of attention must be placed on early screenings and interventions in vocational rehabilitation as well as driving rehabilitation in patients post-SAH.
Significant others or primary caregivers of patients who suffer from SAH are often overlooked in long-term treatment plans. Significant others have a substantial drop in quality of life post-SAH and disruption in psychosocial domains such as social interactions, work, recreation, and emotional behavior [84]. Additionally, they have increased rates of anxiety and depression compared to a control population [21]. Covey et al. analyzed the fear of recurrence of SAH in patients and their significant others and found that the fear of recurrence in the significant others is higher than that of the patients. This fear of recurrence in the significant other was found to impede recovery as it hindered the patient’s work/daily activities, social activities, and health ratings, leading to a decreased HRQoL within the patient [85]. Significant others should not be left out of the picture while developing a model for long-term care. Support measures should be given to ensure that family members of patients are adjusting to life post-SAH.
Support groups may also be beneficial to patients post-SAH. Support groups can act as a mechanism to detect psychological distress early so that patients can be referred to a proper healthcare professional. To our knowledge, only one study has addressed the use of support groups post-SAH. Noble et al. found that psychological distress went mostly undetected within their sample population prior to initiating support groups. Additionally, the authors found that their established support groups drew in distressed patients 2.5 times more than the average post-SAH population. This support group also had a population that had higher rates of anxiety, depression, and PTSD than the average post-SAH population [86]. There is a paucity of data analyzing the outcomes of support groups or the support groups of significant others post–SAH; thus, further studies are needed to elucidate these outcomes.

4.3. Novel Rehabilitative Strategies and Future Directions

New rehabilitative strategies have been explored as novel treatment modalities for individuals recovering from SAH. Recent studies indicate that hyperbaric oxygen therapy, most commonly used for decompression sickness, may inhibit cerebral vasospasm by mitigating inflammation. Through this mechanism, hyperbaric oxygen is thought to reduce post-SAH edema, increase cerebral blood flow, and minimize infarct size. Limitations to using hyperbaric oxygen include access to hyperbaric oxygen chambers and time for treatment. Studies indicate that delayed treatment may worsen cerebral ischemic injury. Future studies are warranted to determine the external factors that may influence the effectiveness of hyperbaric oxygen therapy, such as advanced age, gender, and underlying hypertension [87].
Neuromodulation is a relatively new therapy currently being considered for use in the recovery period following SAH. Neuromodulation is thought to target inflammatory markers released during the ischemic insult associated with SAH. Recent data has suggested that transcranial direct stimulation (tDCS), a specific type of neuromodulatory therapy, may be therapeutically beneficial post-SAH by inducing alterations in cortical excitability and perfusion. In a rodent study, tDCS therapy implemented 3 and 4 days post-SAH reduced the frequency and severity of vasospasm. This encouraging finding suggests that stimulatory therapy may provide further therapeutic benefit to patients recovering from SAH and could be recommended in addition to pharmacological therapy to prevent complications such as vasospasm post-SAH [88].
Like tDCS, trigeminal nerve stimulation (TNS) has been considered to improve post-SAH circulation and prevent delayed cerebral ischemia due to vasospasm and circulatory dysregulation. Shah et al. showed that TNS increases blood vessel lumen diameter, specifically in the internal carotid artery, middle carotid artery, and anterior cerebral artery in rodents post-SAH. As arterial vasospasm is one of the most common complications post-SAH, this increase in vessel diameter may be protective against this complication [89]. While most of the beneficial effects of neuromodulation are appreciated in preclinical studies, two smaller post-SAH clinical studies with cervical transcutaneous electrical neurostimulation (TENS) and tDCS have shown promising results in improving gait imbalance and cerebral vasospasm [90,91].
Despite a non-severe SAH severity, patients may still experience impairments in several domains, which stresses the need for continued long-term support [73]. Information sessions for patients and families about the rehabilitative process and continued follow-up in outpatient clinics should be encouraged prior to discharge [74,92]. The many problems patients face post-SAH emphasize the need for long-term multidisciplinary care. Multidisciplinary care teams may include a primary physician (neurologist or neurosurgeon), a dedicated stroke nurse, a rehabilitation physician, a mental health specialist, an occupational therapist, and a physical therapist [92,93]. Within the clinic, patients should receive physical, cognitive, emotional, return to work, and return to driving screenings regularly to assess milestones (see Figure 1 for the proposed rehabilitation paradigm post-SAH) [35,75]. There is little to no data on mobilization and nutrition strategies ≥ 3 months post-SAH. This area of research should be explored further to improve patient outcomes.

5. Subarachnoid Hemorrhage Prognostic Biomarkers and Imaging Modalities

Ongoing research is being conducted to identify neurological prognostic biomarkers for SAH patients. Many studies have proposed neuro-specific markers in humans that include S100B, glial fibrillary acid protein (GFAP), neuron-specific enolase (NSE), microtubule-associated protein tau (MAPT), neurofilament-light (NF-L), amyloid-B-protein, apolipoprotein E (ApoE), and ubiquitin C terminal hydrolase 1 (UCHL1) [94]. An increase in almost all markers indicated poorer outcomes except for Amyloid-B-protein and ApoE, in which reductions indicated poorer outcomes (Table 1).
Several imaging modalities are also currently being studied as potential prognostic tools to determine outcomes after SAH. Several studies have identified findings that correlate with poorer outcomes in SAH aside from the initial prognostic indicators, such as the size of the hemorrhage. A study by Fragata et al. found that observed increases in apparent diffusion coefficients (ADC) and decreases in fractional anisotropy (FA) correlated with poor functional outcomes following SAH [109]. Another study by Abdel-Tawab et al. found that an increase in mean transit time (MTT) in computed tomographic perfusion (CTP) correlated with an increase in delayed cerebral ischemia and poorer outcomes [110].
Following SAH, there is an increased risk for recurrence [92]. One study compared life expectancy, quality-adjusted life years (QALY), hemorrhage recurrence, and costs associated with the screening strategies. Screening was found not to be cost-effective post-SAH every five years and reduced QALY [111]. The data supported a benefit from CT angiography screening every 3–5 years in post-ictus patients who are female, were young at ictus (≤35–40 years old), had multiple aneurysms, had a family history of SAH or autosomal dominant polycystic kidney disease, and had a decreased QoL due to fear of recurrence [92,111]. Beyond that, it is generally not recommended to mandate screening but to allow the patient to decide after being fully educated on the risks and benefits of screening [92]. While imaging modalities are well-defined for diagnosis, further research into the prognostic value of extensive imaging and biomarkers could provide increased insight into the functional outcomes of SAH patients and help better guide treatment decisions earlier in the course of care.
Although there are no current guidelines for prognostic biomarkers and imaging modalities at the time of this review, there are well-defined prognostic scales currently in use for SAH patients. A common prognostic scale is the Glasgow Coma Scale (GCS), which evaluates eye opening, motor, and verbal responses. Derivatives of the GCS include the World Federation of Neurological Surgeons Committee Scale (WFNS) and the Prognosis on Admission of Aneurysmal Subarachnoid Hemorrhage (PAASH). Both scales show similar predictability in outcomes for SAH patients [112]. The Hunt and Hess grading system is also frequently used. The Hunt and Hess scale classifies SAH in grades 1 to 5 based on presenting symptoms; however, this grading scale has been scrutinized due to its ambiguity and its utility for use in prognosis [113,114]. The Fisher and modified Fisher scales (mFs) are also used and are based on CT findings at the time of admission [115]. These scales only apply to vasospasm risk rather than clinical outcomes. The VASOGRADE scale was recently developed using a combination of the WFNS and mFs to predict better delayed cerebral ischemia (DCI) and provide insight into poorer acute functional outcomes [116]. The Ogilvy and Carter scale was introduced to predict surgical outcomes. The Ogilvy and Carter scale is based on the Hunt and Hess scale, the Fisher scale, and other factors such as the age and size of the aneurysm [117].
Newer scoring models have also been introduced, such as the Poor-grade Aneurysmal Subarachnoid Hemorrhage Prognostic Scoring System (PASHPSS), which integrates mFs, WFNS, age, conservative treatment, DCI, shunt-dependent hydrocephalus, and cerebral herniation [118]. The PASHPSS scale showed promising results in prognostic prediction but has yet to be clinically implemented or further evaluated. Another newer scoring model includes the “TAPS” model, which incorporates mFs, age, WFNS, the Graeb score of intraventricular hemorrhage, white blood cell count, and surgical clipping parameters [119]. The “TAPS” model showed positive results in prognostic predictability and is currently enrolled in a clinical trial to validate these findings (NCT04785976). While these scales exist and are in use clinically, there is much variability in their use by each institution. At the time of this review, there is no standardized prognostic scale solely for SAH, and further research is required.

6. Conclusions

The advancement of SAH treatment means more patients now survive SAH; however, the SAH survivor population is burdened by a high prevalence of neuropsychiatric and cognitive impairments that impact recovery, social and physical independence, and the ability to return to work. Thus, serious attention and rehabilitative strategies are crucial in addressing these treatable medical issues that the SAH survivor faces. Further research into the best rehabilitative approach is also needed to provide effective mechanisms that optimize outcomes post-SAH.

Author Contributions

Conceptualization, B.L.-W. and D.C.N.; writing—original draft preparation, D.C.N., B.D.K., J.D.R., M.A.C. and E.I.; writing—review and editing, B.L.-W. and D.C.N.; supervision B.L.-W.; funding acquisition, B.L.-W. All authors have read and agreed to the published version of the manuscript.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data sharing not applicable.

Conflicts of Interest

All authors declare no competing interests.

References

  1. Bartlett, M.; Bulters, D.; Hou, R. Psychological distress after subarachnoid haemorrhage: A systematic review and meta-analysis. J. Psychosom. Res. 2021, 148, 110559. [Google Scholar] [CrossRef] [PubMed]
  2. Benke, T.; Koylu, B.; Delazer, M.; Trinka, E.; Kemmler, G. Cholinergic treatment of amnesia following basal forebrain lesion due to aneurysm rupture--an open-label pilot study. Eur. J. Neurol. 2005, 12, 791–796. [Google Scholar] [CrossRef] [PubMed]
  3. Powell, J.; Kitchen, N.; Heslin, J.; Greenwood, R. Psychosocial outcomes at three and nine months after good neurological recovery from aneurysmal subarachnoid haemorrhage: Predictors and prognosis. J. Neurol. Neurosurg. Psychiatry 2002, 72, 772–781. [Google Scholar] [CrossRef] [PubMed]
  4. Epprecht, L.; Messerli, M.; Samuel, R.; Seule, M.; Weber, J.; Fournier, J.Y.; Surbeck, W. Sexual Dysfunction After Good-Grade Aneurysmal Subarachnoid Hemorrhage. World Neurosurg. 2018, 111, e449–e453. [Google Scholar] [CrossRef]
  5. Al-Khindi, T.; Macdonald, R.L.; Schweizer, T.A. Cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. Stroke 2010, 41, e519–e536. [Google Scholar] [CrossRef] [Green Version]
  6. Morris, P.G.; Wilson, J.T.; Dunn, L. Anxiety and depression after spontaneous subarachnoid hemorrhage. Neurosurgery 2004, 54, 47–54. [Google Scholar] [CrossRef] [Green Version]
  7. Catapano, J.S.; Rumalla, K.; Koester, S.W.; Winkler, E.A.; Rudy, R.F.; Cole, T.S.; Baranoski, J.F.; Graffeo, C.S.; Srinivasan, V.M.; Jha, R.P.; et al. Incidence and prediction of chronic depression following aneurysmal subarachnoid hemorrhage: A single-center 17-year experience. World Neurosurg. 2022, 171, e206–e212. [Google Scholar] [CrossRef]
  8. Tang, W.K.; Wang, L.; Kwok Chu Wong, G.; Ungvari, G.S.; Yasuno, F.; Tsoi, K.K.F.; Kim, J.S. Depression after Subarachnoid Hemorrhage: A Systematic Review. J. Stroke 2020, 22, 11–28. [Google Scholar] [CrossRef]
  9. Kreiter, K.T.; Rosengart, A.J.; Claassen, J.; Fitzsimmons, B.F.; Peery, S.; Du, Y.E.; Connolly, E.S.; Mayer, S.A. Depressed mood and quality of life after subarachnoid hemorrhage. J. Neurol. Sci. 2013, 335, 64–71. [Google Scholar] [CrossRef]
  10. von Vogelsang, A.C.; Svensson, M.; Wengstrom, Y.; Forsberg, C. Cognitive, physical, and psychological status after intracranial aneurysm rupture: A cross-sectional study of a Stockholm case series 1996 to 1999. World Neurosurg. 2013, 79, 130–135. [Google Scholar] [CrossRef] [Green Version]
  11. Al Yassin, A.; Ouyang, B.; Temes, R. Depression and Anxiety Following Aneurysmal Subarachnoid Hemorrhage Are Associated With Higher Six-Month Unemployment Rates. J. Neuropsychiatry Clin. Neurosci. 2017, 29, 67–69. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  12. Colledge, F.; Brand, S.; Zimmerer, S.; Puhse, U.; Holsboer-Trachsler, E.; Gerber, M. In Individuals Following Aneurysmal Subarachnoid Haemorrhage, Hair Cortisol Concentrations Are Higher and More Strongly Associated with Psychological Functioning and Sleep Complaints than in Healthy Controls. Neuropsychobiology 2017, 75, 12–20. [Google Scholar] [CrossRef] [PubMed]
  13. Kreitschmann-Andermahr, I.; Poll, E.; Hutter, B.O.; Reineke, A.; Kristes, S.; Gilsbach, J.M.; Saller, B. Quality of life and psychiatric sequelae following aneurysmal subarachnoid haemorrhage: Does neuroendocrine dysfunction play a role? Clin. Endocrinol. 2007, 66, 833–837. [Google Scholar] [CrossRef] [PubMed]
  14. Vaswani, M.; Linda, F.K.; Ramesh, S. Role of selective serotonin reuptake inhibitors in psychiatric disorders: A comprehensive review. Prog. Neuropsychopharmacol. Biol. Psychiatry 2003, 27, 85–102. [Google Scholar] [CrossRef]
  15. Renoux, C.; Vahey, S.; Dell’Aniello, S.; Boivin, J.F. Association of Selective Serotonin Reuptake Inhibitors With the Risk for Spontaneous Intracranial Hemorrhage. JAMA Neurol. 2017, 74, 173–180. [Google Scholar] [CrossRef]
  16. Ackermark, P.Y.; Schepers, V.P.; Post, M.W.; Rinkel, G.J.; Passier, P.E.; Visser-Meily, J.M. Longitudinal course of depressive symptoms and anxiety after aneurysmal subarachnoid hemorrhage. Eur. J. Phys. Rehabil. Med. 2017, 53, 98–104. [Google Scholar] [CrossRef]
  17. Hedlund, M.; Zetterling, M.; Ronne-Engstrom, E.; Carlsson, M.; Ekselius, L. Depression and post-traumatic stress disorder after aneurysmal subarachnoid haemorrhage in relation to lifetime psychiatric morbidity. Br. J. Neurosurg. 2011, 25, 693–700. [Google Scholar] [CrossRef] [Green Version]
  18. Visser-Meily, J.M.; Rinkel, G.J.; Vergouwen, M.D.; Passier, P.E.; van Zandvoort, M.J.; Post, M.W. Post-traumatic stress disorder in patients 3 years after aneurysmal subarachnoid haemorrhage. Cerebrovasc. Dis. 2013, 36, 126–130. [Google Scholar] [CrossRef]
  19. Noble, A.J.; Baisch, S.; Mendelow, A.D.; Allen, L.; Kane, P.; Schenk, T. Posttraumatic stress disorder explains reduced quality of life in subarachnoid hemorrhage patients in both the short and long term. Neurosurgery 2008, 63, 1095–1105. [Google Scholar] [CrossRef]
  20. Noble, A.J.; Schenk, T. Posttraumatic stress disorder in the family and friends of patients who have suffered spontaneous subarachnoid hemorrhage. J. Neurosurg. 2008, 109, 1027–1033. [Google Scholar] [CrossRef]
  21. Rueckriegel, S.M.; Baron, M.; Domschke, K.; Neuderth, S.; Kunze, E.; Kessler, A.F.; Nickl, R.; Westermaier, T.; Ernestus, R.I. Trauma- and distress-associated mental illness symptoms in close relatives of patients with severe traumatic brain injury and high-grade subarachnoid hemorrhage. Acta Neurochir. 2015, 157, 1329–1336. [Google Scholar] [CrossRef] [PubMed]
  22. Baisch, S.B.; Schenk, T.; Noble, A.J. What is the cause of post-traumatic stress disorder following subarachnoid haemorrhage? Post-ictal events are key. Acta Neurochir. 2011, 153, 913–922. [Google Scholar] [CrossRef] [PubMed]
  23. Noble, A.J.; Baisch, S.; Covey, J.; Mukerji, N.; Nath, F.; Schenk, T. Subarachnoid hemorrhage patients’ fears of recurrence are related to the presence of posttraumatic stress disorder. Neurosurgery 2011, 69, 323–333. [Google Scholar] [CrossRef]
  24. Rees, P.M.; Fowler, C.J.; Maas, C.P. Sexual function in men and women with neurological disorders. Lancet 2007, 369, 512–525. [Google Scholar] [CrossRef] [PubMed]
  25. Korpelainen, J.T.; Nieminen, P.; Myllyla, V.V. Sexual functioning among stroke patients and their spouses. Stroke 1999, 30, 715–719. [Google Scholar] [CrossRef] [Green Version]
  26. Song, H.; Oh, H.; Kim, H.; Seo, W. Effects of a sexual rehabilitation intervention program on stroke patients and their spouses. NeuroRehabilitation 2011, 28, 143–150. [Google Scholar] [CrossRef]
  27. Monga, T.N.; Lawson, J.S.; Inglis, J. Sexual dysfunction in stroke patients. Arch Phys. Med. Rehabil. 1986, 67, 19–22. [Google Scholar]
  28. Martin, C.O.; Rymer, M.M. Hemorrhagic stroke: Aneurysmal subarachnoid hemorrhage. Mo Med. 2011, 108, 124–127. [Google Scholar]
  29. Aimaretti, G.; Ambrosio, M.R.; Di Somma, C.; Fusco, A.; Cannavo, S.; Gasperi, M.; Scaroni, C.; De Marinis, L.; Benvenga, S.; degli Uberti, E.C.; et al. Traumatic brain injury and subarachnoid haemorrhage are conditions at high risk for hypopituitarism: Screening study at 3 months after the brain injury. Clin. Endocrinol. 2004, 61, 320–326. [Google Scholar] [CrossRef]
  30. Schneider, H.J.; Kreitschmann-Andermahr, I.; Ghigo, E.; Stalla, G.K.; Agha, A. Hypothalamopituitary dysfunction following traumatic brain injury and aneurysmal subarachnoid hemorrhage: A systematic review. JAMA 2007, 298, 1429–1438. [Google Scholar] [CrossRef]
  31. Nussbaum, E.S.; Mikoff, N.; Paranjape, G.S. Cognitive deficits among patients surviving aneurysmal subarachnoid hemorrhage. A contemporary systematic review. Br. J. Neurosurg. 2021, 35, 384–401. [Google Scholar] [CrossRef] [PubMed]
  32. Rowland, M.J.; Garry, P.; Ezra, M.; Corkill, R.; Baker, I.; Jezzard, P.; Westbrook, J.; Douaud, G.; Pattinson, K.T.S. Early brain injury and cognitive impairment after aneurysmal subarachnoid haemorrhage. Sci. Rep. 2021, 11, 23245. [Google Scholar] [CrossRef]
  33. Alfonso, M.; Aftab, S.; Hamadneh, T.; Sherali, N.; Tsouklidis, N. Understanding Cognitive Deficit After Subarachnoid Hemorrhage: A Memory Focused Approach. Cureus 2020, 12, e11513. [Google Scholar] [CrossRef] [PubMed]
  34. Buunk, A.M.; Spikman, J.M.; Metzemaekers, J.D.M.; van Dijk, J.M.C.; Groen, R.J.M. Return to work after subarachnoid hemorrhage: The influence of cognitive deficits. PLoS ONE 2019, 14, e0220972. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Passier, P.E.; Visser-Meily, J.M.; van Zandvoort, M.J.; Post, M.W.; Rinkel, G.J.; van Heugten, C. Prevalence and determinants of cognitive complaints after aneurysmal subarachnoid hemorrhage. Cerebrovasc. Dis. 2010, 29, 557–563. [Google Scholar] [CrossRef]
  36. Shukla, D.P. Outcome and rehabilitation of patients following aneurysmal subarachnoid haemorrhage. J. Neuroanaesth. Crit. Care 2017, 4, S65–S75. [Google Scholar] [CrossRef] [Green Version]
  37. Dubosh, N.M.; Edlow, J.A. Diagnosis and Initial Emergency Department Management of Subarachnoid Hemorrhage. Emerg. Med. Clin. N. Am. 2021, 39, 87–99. [Google Scholar] [CrossRef] [PubMed]
  38. Oddo, M.; Poole, D.; Helbok, R.; Meyfroidt, G.; Stocchetti, N.; Bouzat, P.; Cecconi, M.; Geeraerts, T.; Martin-Loeches, I.; Quintard, H.; et al. Fluid therapy in neurointensive care patients: ESICM consensus and clinical practice recommendations. Intensive Care Med. 2018, 44, 449–463. [Google Scholar] [CrossRef]
  39. van der Jagt, M. Fluid management of the neurological patient: A concise review. Crit. Care 2016, 20, 126. [Google Scholar] [CrossRef] [Green Version]
  40. Rinkel, G.J.E. Hypervolemia in Aneurysmal Subarachnoid Hemorrhage. Stroke 2005, 36, 1104–1105. [Google Scholar] [CrossRef] [Green Version]
  41. Ayling, O.G.S.; Ibrahim, G.M.; Alotaibi, N.M.; Gooderham, P.A.; Macdonald, R.L. Anemia After Aneurysmal Subarachnoid Hemorrhage Is Associated With Poor Outcome and Death. Stroke 2018, 49, 1859–1865. [Google Scholar] [CrossRef] [PubMed]
  42. Marupudi, N.I.; Mittal, S. Diagnosis and Management of Hyponatremia in Patients with Aneurysmal Subarachnoid Hemorrhage. J. Clin. Med. 2015, 4, 756–767. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  43. Schmutzhard, E.; Rabinstein, A.A. Participants in the International Multi-Disciplinary Consensus Conference on the Critical care Management of Subarachnoid, H. Spontaneous subarachnoid hemorrhage and glucose management. Neurocrit. Care 2011, 15, 281–286. [Google Scholar] [CrossRef]
  44. Gharaibeh, K.A.; Brewer, J.M.; Agarwal, M.; Fulop, T. Risk factors, complication and measures to prevent or reverse catastrophic sodium overcorrection in chronic hyponatremia. Am. J. Med. Sci. 2015, 349, 170–175. [Google Scholar] [CrossRef] [PubMed]
  45. Murphy, T.; Dhar, R.; Diringer, M. Conivaptan bolus dosing for the correction of hyponatremia in the neurointensive care unit. Neurocrit. Care 2009, 11, 14–19. [Google Scholar] [CrossRef] [Green Version]
  46. Singer, P.; Blaser, A.R.; Berger, M.M.; Alhazzani, W.; Calder, P.C.; Casaer, M.P.; Hiesmayr, M.; Mayer, K.; Montejo, J.C.; Pichard, C.; et al. ESPEN guideline on clinical nutrition in the intensive care unit. Clin. Nutr. 2019, 38, 48–79. [Google Scholar] [CrossRef] [Green Version]
  47. Kofler, M.; Beer, R.; Marinoni, S.; Schiefecker, A.J.; Gaasch, M.; Rass, V.; Lindner, A.; Lanosi, B.A.; Rhomberg, P.; Pfausler, B.; et al. Early supplemental parenteral nutrition for the achievement of nutritional goals in subarachnoid hemorrhage patients: An observational cohort study. PLoS ONE 2022, 17, e0265729. [Google Scholar] [CrossRef]
  48. Badjatia, N.; Fernandez, L.; Schlossberg, M.J.; Schmidt, J.M.; Claassen, J.; Lee, K.; Connolly, E.S.; Mayer, S.A.; Rosenbaum, M. Relationship between energy balance and complications after subarachnoid hemorrhage. J. Parenter. Enter. Nutr. 2010, 34, 64–69. [Google Scholar] [CrossRef]
  49. Cinotti, R.; Dordonnat-Moynard, A.; Feuillet, F.; Roquilly, A.; Rondeau, N.; Lepelletier, D.; Caillon, J.; Asseray, N.; Blanloeil, Y.; Rozec, B.; et al. Risk factors and pathogens involved in early ventilator-acquired pneumonia in patients with severe subarachnoid hemorrhage. Eur. J. Clin. Microbiol. Infect. Dis. 2014, 33, 823–830. [Google Scholar] [CrossRef]
  50. Alsharif, D.J.; Alsharif, F.J.; Aljuraiban, G.S.; Abulmeaty, M.M.A. Effect of Supplemental Parenteral Nutrition Versus Enteral Nutrition Alone on Clinical Outcomes in Critically Ill Adult Patients: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. Nutrients 2020, 12, 2968. [Google Scholar] [CrossRef]
  51. Nicolo, M.; Heyland, D.K.; Chittams, J.; Sammarco, T.; Compher, C. Clinical Outcomes Related to Protein Delivery in a Critically Ill Population: A Multicenter, Multinational Observation Study. JPEN J. Parenter Enteral. Nutr. 2016, 40, 45–51. [Google Scholar] [CrossRef] [PubMed]
  52. Karic, T.; Roe, C.; Nordenmark, T.H.; Becker, F.; Sorteberg, W.; Sorteberg, A. Effect of early mobilization and rehabilitation on complications in aneurysmal subarachnoid hemorrhage. J. Neurosurg. 2017, 126, 518–526. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  53. Okamura, M.; Konishi, M.; Sagara, A.; Shimizu, Y.; Nakamura, T. Impact of early mobilization on discharge disposition and functional status in patients with subarachnoid hemorrhage: A retrospective cohort study. Medicine 2021, 100, e28171. [Google Scholar] [CrossRef] [PubMed]
  54. Bernhardt, J.; Langhorne, P.; Lindley, R.I.; Thrift, A.G.; Ellery, F.; Collier, J.; Moodie, M.; Dewey, H.; Donnan, G. Efficacy and safety of very early mobilisation within 24 h of stroke onset (AVERT): A randomised controlled trial. Lancet 2015, 386, 46–55. [Google Scholar] [CrossRef] [Green Version]
  55. Haug Nordenmark, T.; Karic, T.; Sorteberg, W.; Sorteberg, A. Predictors of cognitive function in the acute phase after aneurysmal subarachnoid hemorrhage. Acta Neurochir. 2019, 161, 177–184. [Google Scholar] [CrossRef]
  56. Milovanovic, A.; Grujicic, D.; Bogosavljevic, V.; Jokovic, M.; Mujovic, N.; Markovic, I.P. Efficacy of Early Rehabilitation After Surgical Repair of Acute Aneurysmal Subarachnoid Hemorrhage: Outcomes After Verticalization on Days 2-5 Versus Day 12 Post-Bleeding. Turk Neurosurg. 2017, 27, 867–873. [Google Scholar] [CrossRef] [Green Version]
  57. Chen, B.Y. Early tablet-assisted cognitive rehabilitation for aneurysmal subarachnoid hemorrhage: Feasibility of a single-center randomized controlled trial. Neurology 2018, 90, P3.227. [Google Scholar]
  58. Burrows, A.M.; Korumilli, R.; Lanzino, G. How we do it: Acute management of subarachnoid hemorrhage. Neurol. Res. 2013, 35, 111–116. [Google Scholar] [CrossRef]
  59. Norberg, E.; Odenstedt-Herges, H.; Rydenhag, B.; Oras, J. Impact of Acute Cardiac Complications After Subarachnoid Hemorrhage on Long-Term Mortality and Cardiovascular Events. Neurocrit. Care 2018, 29, 404–412. [Google Scholar] [CrossRef] [Green Version]
  60. Mesotten, D.; Preiser, J.C.; Kosiborod, M. Glucose management in critically ill adults and children. Lancet Diabetes Endocrinol. 2015, 3, 723–733. [Google Scholar] [CrossRef]
  61. Rawal, G.; Kumar, R.; Yadav, S.; Singh, A. Anemia in Intensive Care: A Review of Current Concepts. J. Crit. Care Med. 2016, 2, 109–114. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  62. Askenazi, D.J.; Heung, M.; Connor, M.J., Jr.; Basu, R.K.; Cerda, J.; Doi, K.; Koyner, J.L.; Bihorac, A.; Golestaneh, L.; Vijayan, A.; et al. Optimal Role of the Nephrologist in the Intensive Care Unit. Blood Purif. 2017, 43, 68–77. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  63. Terblanche, E. The role of dietitians in critical care. J. Intensive Care Soc. 2019, 20, 255–257. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  64. Moheet, A.M.; Livesay, S.L.; Abdelhak, T.; Bleck, T.P.; Human, T.; Karanjia, N.; Lamer-Rosen, A.; Medow, J.; Nyquist, P.A.; Rosengart, A.; et al. Standards for Neurologic Critical Care Units: A Statement for Healthcare Professionals from The Neurocritical Care Society. Neurocrit. Care 2018, 29, 145–160. [Google Scholar] [CrossRef] [Green Version]
  65. Dodd, J.N.; Hall, T.A.; Guilliams, K.; Guerriero, R.M.; Wagner, A.; Malone, S.; Williams, C.N.; Hartman, M.E.; Piantino, J. Optimizing Neurocritical Care Follow-Up Through the Integration of Neuropsychology. Pediatr. Neurol. 2018, 89, 58–62. [Google Scholar] [CrossRef]
  66. Olkowski, B. Early Mobilization in Aneurysmal Subarachnoid Hemorrhage Accelerates Recovery and Reduces Length of Stay. J. Acute Care Phys. Ther. 2015, 6, 47–55. [Google Scholar] [CrossRef]
  67. Diringer, M.N.; Bleck, T.P.; Claude Hemphill, J., 3rd; Menon, D.; Shutter, L.; Vespa, P.; Bruder, N.; Connolly, E.S., Jr.; Citerio, G.; Gress, D.; et al. Critical care management of patients following aneurysmal subarachnoid hemorrhage: Recommendations from the Neurocritical Care Society’s Multidisciplinary Consensus Conference. Neurocrit. Care 2011, 15, 211–240. [Google Scholar] [CrossRef] [PubMed]
  68. Rabinstein, A.A.; Lanzino, G.; Wijdicks, E.F. Multidisciplinary management and emerging therapeutic strategies in aneurysmal subarachnoid haemorrhage. Lancet Neurol. 2010, 9, 504–519. [Google Scholar] [CrossRef]
  69. Samuels, O.; Webb, A.; Culler, S.; Martin, K.; Barrow, D. Impact of a dedicated neurocritical care team in treating patients with aneurysmal subarachnoid hemorrhage. Neurocrit. Care 2011, 14, 334–340. [Google Scholar] [CrossRef]
  70. Lovelock, C.E.; Rinkel, G.J.; Rothwell, P.M. Time trends in outcome of subarachnoid hemorrhage: Population-based study and systematic review. Neurology 2010, 74, 1494–1501. [Google Scholar] [CrossRef]
  71. Taufique, Z.; May, T.; Meyers, E.; Falo, C.; Mayer, S.A.; Agarwal, S.; Park, S.; Connolly, E.S.; Claassen, J.; Schmidt, J.M. Predictors of Poor Quality of Life 1 Year After Subarachnoid Hemorrhage. Neurosurgery 2016, 78, 256–264. [Google Scholar] [CrossRef]
  72. Nieuwkamp, D.J.; Setz, L.E.; Algra, A.; Linn, F.H.; de Rooij, N.K.; Rinkel, G.J. Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: A meta-analysis. Lancet Neurol. 2009, 8, 635–642. [Google Scholar] [CrossRef] [PubMed]
  73. Sonesson, B.; Kronvall, E.; Saveland, H.; Brandt, L.; Nilsson, O.G. Long-term reintegration and quality of life in patients with subarachnoid hemorrhage and a good neurological outcome: Findings after more than 20 years. J. Neurosurg. 2018, 128, 785–792. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  74. Persson, H.C.; Tornbom, K.; Sunnerhagen, K.S.; Tornbom, M. Consequences and coping strategies six years after a subarachnoid hemorrhage - A qualitative study. PLoS ONE 2017, 12, e0181006. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  75. Passier, P.E.; Visser-Meily, J.M.; Rinkel, G.J.; Lindeman, E.; Post, M.W. Determinants of health-related quality of life after aneurysmal subarachnoid hemorrhage: A systematic review. Qual. Life Res. 2013, 22, 1027–1043. [Google Scholar] [CrossRef]
  76. Visser-Meily, J.M.; Rhebergen, M.L.; Rinkel, G.J.; van Zandvoort, M.J.; Post, M.W. Long-term health-related quality of life after aneurysmal subarachnoid hemorrhage: Relationship with psychological symptoms and personality characteristics. Stroke 2009, 40, 1526–1529. [Google Scholar] [CrossRef] [Green Version]
  77. von Vogelsang, A.C.; Forsberg, C.; Svensson, M.; Wengstrom, Y. Patients Experience High Levels of Anxiety 2 Years Following Aneurysmal Subarachnoid Hemorrhage. World Neurosurg. 2015, 83, 1090–1097. [Google Scholar] [CrossRef]
  78. Lai, P.M.R.; Du, R. Return to Driving Is a Better Predictor of Patient Outcome Than Return to Work After Aneurysmal Subarachnoid Hemorrhage. World Neurosurg. 2020, 144, e285–e295. [Google Scholar] [CrossRef]
  79. Passier, P.E.; Visser-Meily, J.M.; Rinkel, G.J.; Lindeman, E.; Post, M.W. Life satisfaction and return to work after aneurysmal subarachnoid hemorrhage. J. Stroke Cerebrovasc. Dis. 2011, 20, 324–329. [Google Scholar] [CrossRef]
  80. Fertl, E.; Killer, M.; Eder, H.; Linzmayer, L.; Richling, B.; Auff, E. Long-term functional effects of aneurysmal subarachnoid haemorrhage with special emphasis on the patient’s view. Acta Neurochir. 1999, 141, 571–577. [Google Scholar] [CrossRef]
  81. Vetkas, A.; Lepik, T.; Eilat, T.; Ratsep, T.; Asser, T. Emotional health and quality of life after aneurysmal subarachnoid hemorrhage. Acta Neurochir. 2013, 155, 1107–1114. [Google Scholar] [CrossRef]
  82. Buunk, A.M.; Groen, R.J.; Veenstra, W.S.; Spikman, J.M. Leisure and social participation in patients 4-10 years after aneurysmal subarachnoid haemorrhage. Brain Inj. 2015, 29, 1589–1596. [Google Scholar] [CrossRef] [PubMed]
  83. Turi, E.R.; Conley, Y.; Crago, E.; Sherwood, P.; Poloyac, S.M.; Ren, D.; Stanfill, A.G. Psychosocial Comorbidities Related to Return to Work Rates Following Aneurysmal Subarachnoid Hemorrhage. J. Occup. Rehabil. 2019, 29, 205–211. [Google Scholar] [CrossRef] [PubMed]
  84. Hop, J.W.; Rinkel, G.J.; Algra, A.; van Gijn, J. Quality of life in patients and partners after aneurysmal subarachnoid hemorrhage. Stroke 1998, 29, 798–804. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  85. Covey, J.; Noble, A.J.; Schenk, T. Family and friends’ fears of recurrence: Impact on the patient’s recovery after subarachnoid hemorrhage. J. Neurosurg. 2013, 119, 948–954. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  86. Noble, A.J.; Schenk, T. Psychological distress after subarachnoid hemorrhage: Patient support groups can help us better detect it. J. Neurol. Sci. 2014, 343, 125–131. [Google Scholar] [CrossRef]
  87. Wang, Y.; Gao, Y.; Lu, M.; Liu, Y. Long-term functional prognosis of patients with aneurysmal subarachnoid hemorrhage treated with rehabilitation combined with hyperbaric oxygen: Case-series study. Medicine 2020, 99, e18748. [Google Scholar] [CrossRef]
  88. Malinova, V.; Bleuel, K.; Stadelmann, C.; Iliev, B.; Tsogkas, I.; Psychogios, M.N.; Rohde, V.; Mielke, D. The impact of transcranial direct current stimulation on cerebral vasospasm in a rat model of subarachnoid hemorrhage. J. Cereb. Blood Flow Metab. 2021, 41, 2000–2009. [Google Scholar] [CrossRef]
  89. Shah, K.A.; White, T.G.; Powell, K.; Woo, H.H.; Narayan, R.K.; Li, C. Trigeminal Nerve Stimulation Improves Cerebral Macrocirculation and Microcirculation After Subarachnoid Hemorrhage: An Exploratory Study. Neurosurgery 2022, 90, 485–494. [Google Scholar] [CrossRef]
  90. ter Laan, M.; van Dijk, J.M.; Stewart, R.; Staal, M.J.; Elting, J.W. Modulation of cerebral blood flow with transcutaneous electrical neurostimulation (TENS) in patients with cerebral vasospasm after subarachnoid hemorrhage. Neuromodulation 2014, 17, 431–436. [Google Scholar] [CrossRef]
  91. Tonomura, T.; Satow, T.; Hyuga, Y.; Mima, T. Use of transcranial direct current stimulation in poststroke postural imbalance. BMJ Case Rep. 2021, 14. [Google Scholar] [CrossRef] [PubMed]
  92. Rinkel, G.J.; Algra, A. Long-term outcomes of patients with aneurysmal subarachnoid haemorrhage. Lancet Neurol. 2011, 10, 349–356. [Google Scholar] [CrossRef] [PubMed]
  93. Harmsen, W.J.; Ribbers, G.M.; Heijenbrok-Kal, M.H.; Khajeh, L.; Sneekes, E.M.; van Kooten, F.; Neggers, S.; van den Berg-Emons, R.J. Fatigue After Aneurysmal Subarachnoid Hemorrhage Is Highly Prevalent in the First-Year Postonset and Related to Low Physical Fitness: A Longitudinal Study. Am. J. Phys. Med. Rehabil. 2019, 98, 7–13. [Google Scholar] [CrossRef] [PubMed]
  94. Hong, C.M.; Tosun, C.; Kurland, D.B.; Gerzanich, V.; Schreibman, D.; Simard, J.M. Biomarkers as outcome predictors in subarachnoid hemorrhage--a systematic review. Biomarkers 2014, 19, 95–108. [Google Scholar] [CrossRef]
  95. Kedziora, J.; Burzynska, M.; Gozdzik, W.; Kubler, A.; Kobylinska, K.; Adamik, B. Biomarkers of Neurological Outcome After Aneurysmal Subarachnoid Hemorrhage as Early Predictors at Discharge from an Intensive Care Unit. Neurocrit. Care 2021, 34, 856–866. [Google Scholar] [CrossRef]
  96. Kedziora, J.; Burzynska, M.; Gozdzik, W.; Kubler, A.; Uryga, A.; Kasprowicz, M.; Adamik, B. Brain-Specific Biomarkers as Mortality Predictors after Aneurysmal Subarachnoid Haemorrhage. J. Clin. Med. 2020, 9, 4117. [Google Scholar] [CrossRef]
  97. Oertel, M.; Schumacher, U.; McArthur, D.L.; Kastner, S.; Boker, D.K. S-100B and NSE: Markers of initial impact of subarachnoid haemorrhage and their relation to vasospasm and outcome. J. Clin. Neurosci. 2006, 13, 834–840. [Google Scholar] [CrossRef]
  98. Tawk, R.G.; Grewal, S.S.; Heckman, M.G.; Rawal, B.; Miller, D.A.; Edmonston, D.; Ferguson, J.L.; Navarro, R.; Ng, L.; Brown, B.L.; et al. The Relationship Between Serum Neuron-Specific Enolase Levels and Severity of Bleeding and Functional Outcomes in Patients With Nontraumatic Subarachnoid Hemorrhage. Neurosurgery 2016, 78, 487–491. [Google Scholar] [CrossRef]
  99. Gyldenholm, T.; Hvas, C.L.; Hvas, A.M.; Hviid, C.V.B. Serum glial fibrillary acidic protein (GFAP) predicts outcome after intracerebral and subarachnoid hemorrhage. Neurol. Sci. 2022, 43, 6011–6019. [Google Scholar] [CrossRef]
  100. Katsanos, A.H.; Makris, K.; Stefani, D.; Koniari, K.; Gialouri, E.; Lelekis, M.; Chondrogianni, M.; Zompola, C.; Dardiotis, E.; Rizos, I.; et al. Plasma Glial Fibrillary Acidic Protein in the Differential Diagnosis of Intracerebral Hemorrhage. Stroke 2017, 48, 2586–2588. [Google Scholar] [CrossRef]
  101. Helbok, R.; Schiefecker, A.; Delazer, M.; Beer, R.; Bodner, T.; Pfausler, B.; Benke, T.; Lackner, P.; Fischer, M.; Sohm, F.; et al. Cerebral tau is elevated after aneurysmal subarachnoid haemorrhage and associated with brain metabolic distress and poor functional and cognitive long-term outcome. J. Neurol. Neurosurg. Psychiatry 2015, 86, 79–86. [Google Scholar] [CrossRef] [PubMed]
  102. Zanier, E.R.; Refai, D.; Zipfel, G.J.; Zoerle, T.; Longhi, L.; Esparza, T.J.; Spinner, M.L.; Bateman, R.J.; Brody, D.L.; Stocchetti, N. Neurofilament light chain levels in ventricular cerebrospinal fluid after acute aneurysmal subarachnoid haemorrhage. J. Neurol. Neurosurg. Psychiatry 2011, 82, 157–159. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  103. Garland, P.; Morton, M.; Zolnourian, A.; Durnford, A.; Gaastra, B.; Toombs, J.; Heslegrave, A.J.; More, J.; Zetterberg, H.; Bulters, D.O.; et al. Neurofilament light predicts neurological outcome after subarachnoid haemorrhage. Brain 2021, 144, 761–768. [Google Scholar] [CrossRef] [PubMed]
  104. Lewis, S.B.; Wolper, R.; Chi, Y.Y.; Miralia, L.; Wang, Y.; Yang, C.; Shaw, G. Identification and preliminary characterization of ubiquitin C terminal hydrolase 1 (UCHL1) as a biomarker of neuronal loss in aneurysmal subarachnoid hemorrhage. J. Neurosci. Res. 2010, 88, 1475–1484. [Google Scholar] [CrossRef]
  105. Bsat, S.; Chanbour, H.; Bsat, A.; Alomari, S.; Moussalem, C.; Houshiemy, M.N.E.; Omeis, I. Clinical utility of degradomics as predictors of complications and clinical outcome in aneurysmal subarachnoid hemorrhage. J. Integr. Neurosci. 2021, 20, 489–497. [Google Scholar] [CrossRef]
  106. Joswig, H.; Korte, W.; Fruh, S.; Epprecht, L.; Hildebrandt, G.; Fournier, J.Y.; Stienen, M.N. Neurodegenerative cerebrospinal fluid biomarkers tau and amyloid beta predict functional, quality of life, and neuropsychological outcomes after aneurysmal subarachnoid hemorrhage. Neurosurg. Rev. 2018, 41, 605–614. [Google Scholar] [CrossRef]
  107. Kay, A.; Petzold, A.; Kerr, M.; Keir, G.; Thompson, E.; Nicoll, J. Temporal alterations in cerebrospinal fluid amyloid beta-protein and apolipoprotein E after subarachnoid hemorrhage. Stroke 2003, 34, e240–e243. [Google Scholar] [CrossRef] [Green Version]
  108. Kay, A.; Petzold, A.; Kerr, M.; Keir, G.; Thompson, E.; Nicoll, J. Decreased cerebrospinal fluid apolipoprotein E after subarachnoid hemorrhage: Correlation with injury severity and clinical outcome. Stroke 2003, 34, 637–642. [Google Scholar] [CrossRef] [Green Version]
  109. Fragata, I.; Alves, M.; Papoila, A.L.; Ferreira, P.; Nunes, A.P.; Moreira, N.C.; Canhao, P. Prediction of clinical outcome in subacute subarachnoid hemorrhage using diffusion tensor imaging. J. Neurosurg. 2018, 1–9. [Google Scholar] [CrossRef] [Green Version]
  110. Abdel-Tawab, M. Prognostic factors of delayed cerebral ischemia after subarachnoid hemorrhage including CT perfusion: A prospective cohort study. Egypt. J. Radiol. Nucl. Med. 2020, 51, 61. [Google Scholar] [CrossRef]
  111. Wermer, M.J.; Koffijberg, H.; van der Schaaf, I.C.; Group, A.S. Effectiveness and costs of screening for aneurysms every 5 years after subarachnoid hemorrhage. Neurology 2008, 70, 2053–2062. [Google Scholar] [CrossRef] [PubMed]
  112. van Heuven, A.W.; Dorhout Mees, S.M.; Algra, A.; Rinkel, G.J. Validation of a prognostic subarachnoid hemorrhage grading scale derived directly from the Glasgow Coma Scale. Stroke 2008, 39, 1347–1348. [Google Scholar] [CrossRef] [PubMed]
  113. Rosen, D.S.; Macdonald, R.L. Subarachnoid hemorrhage grading scales: A systematic review. Neurocrit. Care 2005, 2, 110–118. [Google Scholar] [CrossRef] [PubMed]
  114. Oshiro, E.M.; Walter, K.A.; Piantadosi, S.; Witham, T.F.; Tamargo, R.J. A new subarachnoid hemorrhage grading system based on the Glasgow Coma Scale: A comparison with the Hunt and Hess and World Federation of Neurological Surgeons Scales in a clinical series. Neurosurgery 1997, 41, 140–147; discussion 147–148. [Google Scholar] [CrossRef]
  115. Claassen, J.; Bernardini, G.L.; Kreiter, K.; Bates, J.; Du, Y.E.; Copeland, D.; Connolly, E.S.; Mayer, S.A. Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: The Fisher scale revisited. Stroke 2001, 32, 2012–2020. [Google Scholar] [CrossRef]
  116. de Oliveira Manoel, A.L.; Jaja, B.N.; Germans, M.R.; Yan, H.; Qian, W.; Kouzmina, E.; Marotta, T.R.; Turkel-Parrella, D.; Schweizer, T.A.; Macdonald, R.L.; et al. The VASOGRADE: A Simple Grading Scale for Prediction of Delayed Cerebral Ischemia After Subarachnoid Hemorrhage. Stroke 2015, 46, 1826–1831. [Google Scholar] [CrossRef] [Green Version]
  117. Ogilvy, C.S.; Carter, B.S. A proposed comprehensive grading system to predict outcome for surgical management of intracranial aneurysms. Neurosurgery 1998, 42, 959–968. [Google Scholar] [CrossRef]
  118. Shen, J.; Yu, J.; Huang, S.; Mungur, R.; Huang, K.; Pan, X.; Yu, G.; Xie, Z.; Zhou, L.; Liu, Z.; et al. Scoring Model to Predict Functional Outcome in Poor-Grade Aneurysmal Subarachnoid Hemorrhage. Front. Neurol. 2021, 12, 601996. [Google Scholar] [CrossRef]
  119. Li, R.; Lin, F.; Chen, Y.; Lu, J.; Han, H.; Ma, L.; Zhao, Y.; Yan, D.; Li, R.; Yang, J.; et al. A 90-Day Prognostic Model Based on the Early Brain Injury Indicators after Aneurysmal Subarachnoid Hemorrhage: The TAPS Score. Transl. Stroke Res. 2022. [Google Scholar] [CrossRef]
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Figure 1. The proposed rehabilitative paradigm for SAH patients. Image credit: Biorender.
Figure 1. The proposed rehabilitative paradigm for SAH patients. Image credit: Biorender.
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Table
Table 1. Prognostic biomarkers and outcomes correlation in the setting of SAH.
Table 1. Prognostic biomarkers and outcomes correlation in the setting of SAH.
BiomarkerCommentsStudy References
S100BIncreased; correlated to poorer outcomes in the acute setting.[95,96]
NSEIncreased; correlated to poorer outcomes such as increased mortality and vasospasm.[97,98]
GFAPIncreased; correlated to higher mortality and poor functional outcomes.[99,100]
MAPTIncreased; correlated to poorer outcomes in the acute setting, increased hypoxic brain injury, and poor functional outcomes at 12 months.[95,101]
NF-LIncreased; correlated to early cerebral ischemia and poor neurological outcome at 6 months.[102,103]
UCHL1Increased; sub-acute period correlated with increased neuronal loss and poorer outcomes.[104,105]
Amyloid-B-proteinDecreased; correlated to poorer long-term functional outcomes. [106,107]
ApoEDecreased; correlated to increased inflammation and poorer outcomes. [107,108]
Abbreviations: glial fibrillary acid protein (GFAP), neuron-specific enolase (NSE), microtubule-associated protein tau (MAPT), neurofilament-light (NF-L), apolipoprotein E (ApoE), and ubiquitin C terminal hydrolase 1 (UCHL1).
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Nwafor, D.C.; Kirby, B.D.; Ralston, J.D.; Colantonio, M.A.; Ibekwe, E.; Lucke-Wold, B. Neurocognitive Sequelae and Rehabilitation after Subarachnoid Hemorrhage: Optimizing Outcomes. J. Vasc. Dis. 2023, 2, 197-211. https://doi.org/10.3390/jvd2020014

AMA Style

Nwafor DC, Kirby BD, Ralston JD, Colantonio MA, Ibekwe E, Lucke-Wold B. Neurocognitive Sequelae and Rehabilitation after Subarachnoid Hemorrhage: Optimizing Outcomes. Journal of Vascular Diseases. 2023; 2(2):197-211. https://doi.org/10.3390/jvd2020014

Chicago/Turabian Style

Nwafor, Divine C., Brandon D. Kirby, Jacob D. Ralston, Mark A. Colantonio, Elochukwu Ibekwe, and Brandon Lucke-Wold. 2023. "Neurocognitive Sequelae and Rehabilitation after Subarachnoid Hemorrhage: Optimizing Outcomes" Journal of Vascular Diseases 2, no. 2: 197-211. https://doi.org/10.3390/jvd2020014

APA Style

Nwafor, D. C., Kirby, B. D., Ralston, J. D., Colantonio, M. A., Ibekwe, E., & Lucke-Wold, B. (2023). Neurocognitive Sequelae and Rehabilitation after Subarachnoid Hemorrhage: Optimizing Outcomes. Journal of Vascular Diseases, 2(2), 197-211. https://doi.org/10.3390/jvd2020014

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