Clinical Neurology and Neurosurgery Supports open access Submit your article Menu Search in this journal Volume 208 September 2021 Download full issue Previous vol/issue Next vol/issue Receive an update when the latest issues in this journal are published Sign in to set up alerts Full text access Editorial Board Article 106927 Download PDF Reviews Review article Full text access Progressive encephalomyelitis with rigidity: A Taiwanese case and review of literature Anna Chang, Kuan-yu Lin, Kai-Ju Chuang, Patrick Waters, ... Wei-Hung Chen Article 106807 Download PDF Review article Article preview Full text access Chronic subdural hematoma-induced parkinsonism: A systematic review Achmad Fahmi, Heru Kustono, Komang Sena Adhistira, Heri Subianto, ... 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LOUIS Clinical Neurology and Neurosurgery 208 (2021) 106826 Contents lists available at ScienceDirect Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro Chronic subdural hematoma-induced parkinsonism: A systematic review Achmad Fahmi a, b, *, Heru Kustono a, b, Komang Sena Adhistira a, b, Heri Subianto a, b, Budi Utomo c, Agus Turchan a, b a Department of Neurosurgery, Faculty of Medicine, Universitas Airlangga, Surabaya, Indonesia Dr. Soetomo General Academic Hospital, Surabaya, Indonesia c Department of Public Health and Preventive Medicine, Faculty of Medicine, Universitas Airlangga, Surabaya, Indonesia b A R T I C L E I N F O A B S T R A C T Keywords: Chronic subdural hematoma Parkinsonism Parkinson’s disease Background: Chronic subdural hematoma (CSDH) is one of the most common neurosurgical cases, especially in elderly individuals. Secondary parkinsonism due to CSDH is a rare entity. The mechanism of parkinsonism symptoms in chronic subdural hematoma has been suggested to include direct mechanical compression of the basal ganglia due to hematoma or indirectly through brain structure changes due to space lesions and vascular disorders. Surgery on the subdural hematoma provides a favorable outcome for parkinsonism symptoms. Objectives: To systematically review the literature on CSDH-induced parkinsonism. Search methods: This is a systematic review on case reports. Literature search was performed using the predefined keywords on PubMed, ProQuest, and Google Scholar. We also provided our own case report and compared it with published studies. Result: Sixteen cases from 13 case reports/series were identified, predominantly consisting of male patients with the mean age of 66.5 ± 9.73 years. The most common symptoms were rigidity, gait disturbance, and bradyki­ nesia, observed in 12 (75%) cases each. The second and third most common symptoms were tremor (11; 68.75%) and facial masking (8; 50%), respectively. Other reported symptoms were dysphasia (3; 18.75%), dysarthria (3; 18.75%), and urinary incontinence (2; 12. 5%). Time gap between the symptom onset and CSDH diagnosis and unilateral location seemed to influence the outcome. Conclusion: Only 16 CSDH-induced parkinsonism were identified since the 1960s. This condition is thought to occur due to basal ganglia compression. Surgery on the subdural hematoma provides a favorable outcome for parkinsonism symptoms. Timely CSDH diagnosis might yield better outcome. However, further research on CSDH-induced parkinsonism is needed, especially in the mechanisms and treatment outcomes. 1. Introduction Chronic subdural hematoma (CSDH) is a common neurosurgical diagnosis among elderly individuals [1]. This condition could occur following a trivial head trauma, and thus, patients usually cannot recall such event ever happening [2]. Various CSDH symptoms range from asymptomatic to the presence of neurological deficits, such as speech and motor [3]. CSDH could rarely cause parkinsonism [4]. The underlying mecha­ nism of CSDH-induced parkinsonism has not been well understood. Mass effect on the basal ganglia [5] or the midbrain [6] might decrease the number of dopaminergic receptors and nigro-striatal dopaminergic pathway, respectively. To date, this type of secondary parkinsonism has been described in the limited number of publications, predominantly in the form of case reports. Therefore, this study aimed to review the general characteris­ tics, symptoms, onset, and outcomes of CSDH-induced parkinsonism based on the available published case reports. 2. Material and methods 2.1. General information and literature search strategy Studies were selected using the Preferred Reporting Items for Sys­ tematic Review and Meta-Analysis Protocol method guideline. Data were collected from PubMed, Sciencedirect, Springer, and Cochrane. * Correspondence to: Faculty of Medicine Universitas Airlangga, Dr. Soetomo General Academic Hospital, Jalan Mayjend Prof. Dr. Moestopo No. 6 - 8, Surabaya 60286, Indonesia. E-mail address: achmad.fahmi@fk.unair.ac.id (A. Fahmi). https://doi.org/10.1016/j.clineuro.2021.106826 Received 12 October 2020; Received in revised form 29 June 2021; Accepted 18 July 2021 Available online 21 July 2021 0303-8467/© 2021 Elsevier B.V. All rights reserved. A. Fahmi et al. Clinical Neurology and Neurosurgery 208 (2021) 106826 2.3. Information source and search strategy Table 1 Search strategy. No Keywords 1 2 3 4 5 6 7 8 9 10 Chronic Subdural Hematoma Subdural Hematoma “Hematoma, Subdural, Chronic” [Mesh] “Hematoma, Subdural, Intracranial” [Mesh] Parkinsonism Parkinson Disease “Parkinson Disease, Secondary” [Mesh] “Parkinson Disease” [Mesh] “Parkinsonian Disorders” [Mesh] (#1 OR #2 OR #3 OR #4) AND (#5 OR #6 OR #7 OR #8 OR #9) We conducted a systematic search on the literature to identify rele­ vant articles using PubMed, ProQuest, and Google Scholar using the following keywords in Table 1. 2.4. Study selection All potentially included articles were screened in two eligibility stages. In the first assessment stage, titles and abstracts of potentially pertinent articles were independently screened by two authors (HK and SA). For abstracts that met the inclusion criteria, the full text was retrieved and independently reviewed by the same authors in the second assessment stage. Contretemps and technical uncertainties were dis­ cussed and resolved among review authors (HK, SA, AF, HS, BU and AT). 2.2. Eligibility criteria Articles included in this review were case reports of patients without age or origin restriction who had CSDH with parkinsonism symptoms. Only articles written in English were accepted for this review. For in­ clusion, published articles must report CSDH, parkinsonism symptoms, surgery, outcomes, and follow-up patients. All articles as well as reviews, editorials, commentaries, or publica­ tions not reporting patients outcome were excluded. Studies performing analysis without description of individual patients were excluded. All case reports and case series on patients with history of Parkinson’s disease (PD) were further excluded. 2.5. Data collection The data collection protocol was designated and agreed before starting the project. Bibliographic data, patient’s management, outcome feature, and follow-up outcome were extracted. Two authors (HK and SA) independently extracted the data from selected studies. Data were jointly reconciled, and disputes and technical uncertainties were dis­ cussed and resolved among review authors (HK, SA, AF, HS, BU and AT). Fig. 1. PRISMA flow diagram of article search, screening, eligibility, and inclusion. 2 A. Fahmi et al. Clinical Neurology and Neurosurgery 208 (2021) 106826 incontinence (2; 12.5%) (Table 3). We tried to calculate the risk ratio of SDH location and its outcome. Bilateral CSDH resulted in minimally symptomatic outcome in two cases and free of symptoms in five cases. Unilateral CSDH resulted in mini­ mally symptomatic outcome in four cases and free of symptoms in five cases. Risk ratio (RR) calculation showed that unilateral CSDH is 1.5, more likely to result in partial recovery. We also tried to dichotomize the time gap of symptom onset to CSDH diagnosis into ≤1 month and >1 month. Three symptomatic patients were classified in the ≤1-month group and 7 patients who were asymptomatic upon follow-ups. In the >1-month group, three and two patients were symptomatic and asymptomatic, respectively. One patient did not mention the time gap between symptom onset and CSDH diag­ nosis. The RR calculation showed that longer time gap between symp­ toms and diagnosis doubled the risk of partial recovery. Table 2 Participant characteristic of all included studies. Mean age (years) Site of lesion n (%) Bilateral Right-sided Left-sided Traumatic event n (%) Known Denied Symptoms Tremor Rigidity Gait disturbance Dysphasia Facial masking Bradykinesia Urinary incontinence Dysarthria Time to symptoms n (%) ≤1 month >1 month Unreported Symptoms to diagnosis n (%) ≤1 month >1 month Unreported Treatment n (%) Burr hole drainage Craniotomy Burr hole drainage + medication Craniotomy + medication Observation Not reported Outcome Minimally symptomatic/partial recovery No symptoms Duration of follow-up (median, range) 66.5 ± 9.73 7 (43.75) 5 (31.25) 4 (25) 10 (62.5) 6 (37.5) 11 (68.75) 12 (75) 12 (75) 3 (18.75) 8 (50) 12 (75) 2 (12.5) 3 (18.75) 4. Discussion 6 (37.5) 4 (25) 6 (37.5) Parkinsonism due to CSDH quite rarely occurs. We had experienced treating such patient. A 76-year-old man presents with rigidity and tremors in both arms and legs for 1 month before admission. He also complained of sluggish movement of both arms and legs. Complaints are continuously getting worse. The Unified Parkinson Disease Rating Scale (UPDRS) shows a score of 100. In the last 1 month, the patient fell and hit his head; however, he did not remember the exact time of and fre­ quency of occurrences. Other complaints such as headache, nausea, vomiting, seizures, and decreased consciousness were not observed. No history of parkinsonism was observed. Patient also had no history of Parkinson medication. The patient then underwent a magnetic resonance imaging (MRI) of the head, revealing a bilateral chronic subdural hematoma (CSDH) (Fig. 2). We decided to perform bilateral burr-hole drainage craniotomy. Postoperative computed tomography (CT) scan evaluation shows decreased hematoma size (Fig. 3). Parkinson-like symptoms disappeared immediately after the surgery, and the UPDRS shows a score of 24. After a 2-week hospitalization, the patient was discharged without any antiParkinson drugs administered. Postoperative follow-up shows com­ plete resolution of all Parkinson-like symptoms. The UPDRS score re­ mains at 24, until the 5-year postoperative follow-up. The 2-year postoperative MRI examination shows no residual hematoma left (Fig. 4). Parkinsonism consists of several extrapyramidal signs, characterized by muscle rigidity, tremor, bradykinesia, and loss of postural reflexes. The most common cause of parkinsonism is idiopathic Parkinson’s dis­ ease, whereas the secondary ones include drug exposure, infection, and trauma, constituting approximately 14–16% of all cases, especially in patients aged ≥40 years [10,14–18]. Acute onset of parkinsonism or worsening of pre-existing parkin­ sonism is a rare CSDH manifestation, but is significantly correlated because both parkinsonism and CSDH are related with elderly in­ dividuals [9,16]. Trauma is an important factor in the CSDH occurrence in elderly individuals. Old age is associated with cerebral atrophy and increased venous fragility, the major predisposing factors for CSDH, even after the minor head injury. Nevertheless, a direct head injury is not reported in 30–50% of studies [19,20]. CSDH itself may have various movement disorder manifestations, such as chorea [21], dystonia [22], and parkinsonism [13,17]. Movement disorders are occasionally asso­ ciated with chronic subdural hematomas [9]. The interval between initial symptoms and CSDH diagnosis ranged from 1 week to 1 year (mean interval, 8 weeks) in a study [10]. The pathomechanism leading to parkinsonism in CSH remains unclear, and several mechanisms can be postulated. Direct mechanical pressure on the basal ganglia, either directly by the overlaying hematoma or through torsion and brain structure displacement, has been postulated [7,15]. Compression may result in decreased number of dopaminergic receptors in the striatum, and a disturbance of nigrostriatal pathways and striatum 10 (62.5) 5 (31.25) 1 (6.25) 8 (50) 3 (18.75) 2 (12.5) 1 (6.25) 1 (6.25) 1 (6.25) 6 (37.5) 10 (62.5) 3 months (1 week–4 years) 3. Results 3.1. Search result Our search strategy yields 12 case reports and one case series pub­ lished from 1963 to 2017. The detailed exclusion process of search re­ sults can be observed in Fig. 1. 3.2. Summary of studies The included studies comprised 16 cases of CSDH-induced parkin­ sonism, and 12 (75%) of which occurred in male. The youngest patient aged 38 years [7], whereas the oldest aged 83 years [8]. The mean age was 66.5 ± 9.73 years (Table 2). Hematoma in seven of these cases were bilateral, five were on the left side, and the rest were on the right side. In ten (62.5%) of 16 cases, the traumatic event leading to CSDH could be identified, whereas the other six (37.5%) could not recall such event. The time gap between known traumatic event to the symptom onset ranged from 1 week to 6 months. Conversely, the CSDH diagnosis was known as early as 1 week to as late as 5 months since the symptom onset. Burr hole drainage and craniotomy were performed in eight (50%) and three (18.75%) studies, respectively. The presentation of CSDH can occur in patients with confirmed PD, that we did not include it in the CSDH-induced parkinsonism group [9,10]. One case had combined levodopa and craniotomy [11]. One case unfortunately did not specif­ ically mention the performed surgical procedure [12], whereas the other one decided to only observe the patient without any intervention [13]. The most common symptoms were rigidity, gait disturbance, and bradykinesia, as reported in 12 (75%) of the cases each. The second and third most common symptoms were tremor (11; 68.75%) and facial masking (8; 50%), respectively. Other reported symptoms were dysphasia (3; 18.75%), dysarthria (3; 18.75%), and urinary 3 A. Fahmi et al. Clinical Neurology and Neurosurgery 208 (2021) 106826 Table 3 Summary of findings of included studies. No Author Participants Sex Age (year) 1 Samiy, 1963 M 52 2 Sandyk, 1983 F 38 3 Accardi, 1985 M 48 4 Krul, 1987 M 83 5 Pau, 1989 F 60 6 Hageman, 1994 M 66 7 Sunada, 1996 M 75 8 Wiest, 1999 M 63 9 Suman, 2006 M 81 10 Park, 2009 M 78 11 Bostantjopoulou, 2009 F 65 12 GelabertGonzalez, 2012 M 71 M 68 M 77 F 59 M 80 13 Guppy, 2017 Symptoms Tremor, rigidity, gait disturbance, dysphasia. Tremor, rigidity, gait disturbance, facial masking, dysphasia, bradykinesia Tremor, rigidity, gait disturbance, bradykinesia Tremor, rigidity, gait disturbance, facial masking, dysphasia, bradykinesia, urinary incontinence. Rigidity, bradykinesia Tremor, facial masking, dysarthria, bradykinesia Tremor, rigidity, gait disturbance, facial masking Tremor, rigidity, gait disturbance, facial masking, dysarthria, bradykinesia Rigidity, gait disturbance Tremor, rigidity, gait disturbance, facial masking, dysarthria, bradykinesia Rigidity, gait disturbance, facial masking, bradykinesia Tremor, rigidity, bradykinesia Tremor, gait disturbance, bradykinesia Rigidity, gait disturbance Tremor, facial masking, bradykinesia Gait disturbance, urinary incontinence, bradykinesia Diagnosis History of trauma Trauma to onset of symptoms Treatment Onset of Symptoms to Diagnosis of CSDH Outcome Symptom Duration of followup CSDH (L) Denied n/a Craniotomy 4 months Minimal 3 months CSDH (R) Denied n/a Craniotomy 3 weeks None 3 months Bilateral CSDH Denied n/a Surgery, not specifically mentioned 5 months Minimal 3 months Bilateral Frontal CSDH Yes 1 week Burr hole 3 weeks Partial recovery n/a CSDH (R) Yes 1 month Craniotomy 1 month Minimal 3 months CSDH (L) Denied n/a Observation a few months Minimal 3 months CSDH (L) Yes 1 month Levodopa 3 months + Craniotomy 1 month None 3 months CSDH (R) Yes 1 week Pre-op Levodopa 3 × 250 mg + Burr hole n/a None 4 weeks Bilateral Frontoparietal CSDH CSDH (L) Yes 2 months Burr hole 2 weeks None 1 weeks Yes 3 months Burr hole 2 weeks Minimal 3 weeks Bilateral CSDH Yes 45 days Burr hole 1 weeks None 1 months Bilateral Frontoparietal CSDH CSDH (L) Yes 1 week Pre-op Levodopa (20 days) + Burr hole 35 days None 2 months Denied n/a Burr hole 1 month None 3 months Bilateral CSDH Yes 1 month Burr hole 2 weeks None 6 months CSDH (R) Denied n/a Burr hole 7 weeks None 4 weeks Bilateral CSDH Yes 6 weeks Burr hole 2 weeks None 4 years and lead to onset of a parkinsonian syndrome. Reduction of dopami­ nergic receptors has been reported in a patient with parkinsonism sec­ ondary to an intracranial tumor who did not benefit from levodopa therapy [9]. Midbrain compression from the transtentorial uncal her­ niation following the brain shift has also been postulated [3]. Positron emission tomography (PET) and diffusion tensor imaging (DTI) MRI might be helpful to uncover the mechanism in the future. Transient circulatory disturbances of basal ganglion structures could be caused by anterior choroidal artery displacement and compression. Exploration about glymphatics and brain lymphatics also needed. For the compres­ sive theory, all patients rapidly recovered after the subdural hematoma evacuation and displacement disappearance of the hemisphere [7]. However, the rarity of parkinsonism due to CSH has led to the hypoth­ esis that these particular patients may have preclinical nigrostriatal dysfunction, and therefore, they cannot compensate with further insults to the basal ganglia [13,23]. 4 A. Fahmi et al. Clinical Neurology and Neurosurgery 208 (2021) 106826 Fig. 4. Two-year postoperative brain MRI examination shows a small residual of hematoma. Fig. 2. Preoperative brain MRI examination shows a bilateral crescent-shaped hyperdense lesion under the dura mater that compresses both hemispheres of the cortex, suggesting a bilateral chronic subdural hematoma (CSDH). not take any anti-parkinsonism medications postoperatively until 5years follow-up. Surgical evacuation of the hematoma has become the gold standard for patients with CSDH, with or without parkinsonism symptoms, and these patients have demonstrated rapid symptom improvement in patients postoperatively [7]. Long-term evaluation is required in these patients, due to the theory of preclinical nigrostriatal dysfunction in patients with parkinsonism in CSDH. Our patients were subjected to periodic follow-up and brain MRI 2-years postoperatively (Fig. 4). To evaluate the signs and symptoms of Parkinson’s disease in these patients, a thorough assessment, including regular UPDRS scoring as performed in our patient, is necessary [13,23]. 4.1. Limitation Limitation of this review relates to exclusion of case reports and case series not in English or Bahasa. Moreover, we might have missed few case reports because relevant search terms may not be found in titles or abstracts. In this study, the conclusions are also found to be limited due to the small number of identified articles. Another limitation of this review is that the outcome assessment was unclear, as only one case report used the UPDRS to assess the outcome. 5. Conclusion Only 16 CSDH-induced parkinsonisms were identified since the 1960s. This condition is thought to occur due to basal ganglia compression. Surgery on the chronic subdural hematoma provides a favorable outcomes on alleviating parkinsonism symptoms. Timely diagnosis of CSDH might result in better outcomes. To screen any CSDHinduced parkinsonism, we propose to perform CT Scan or MRI in every patient with parkinsonism. Further research is needed on CSDH-induced parkinsonism is needed, especially in the mechanisms and treatment outcomes. Fig. 3. Postoperative head CT scan shows the drainage tube placed in the bilateral subdural space, decreasing the hematoma size. A, Axial CT scan; B, Three-dimensional reconstruction. Our patient presented with an extremely new onset, and rapidly progressive symmetrical parkinsonism that affects the whole body. This patient was suspected with CSDH due to history of head impacts for the last 1 month. 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