Sport-related structural brain injury associated with arachnoid cysts: a systematic review and quantitative analysis

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OBJECTIVE

Arachnoid cysts (ACs) are congenital lesions bordered by an arachnoid membrane. Researchers have postulated that individuals with an AC demonstrate a higher rate of structural brain injury after trauma. Given the potential neurological consequences of a structural brain injury requiring neurosurgical intervention, the authors sought to perform a systematic review of sport-related structural-brain injury associated with ACs with a corresponding quantitative analysis.

METHODS

Titles and abstracts were searched systematically across the following databases: PubMed, Embase, CINAHL, and PsycINFO. The review was conducted in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement. Peer-reviewed case reports, case series, or observational studies that reported a structural brain injury due to a sport or recreational activity (hereafter referred to as sport-related) with an associated AC were included. Patients were excluded if they did not have an AC, suffered a concussion without structural brain injury, or sustained the injury during a non–sport-related activity (e.g., fall, motor vehicle collision). Descriptive statistical analysis and time to presentation data were summarized. Univariate logistic regression models to assess predictors of neurological deficit, open craniotomy, and cystoperitoneal shunt were completed.

RESULTS

After an initial search of 994 original articles, 52 studies were found that reported 65 cases of sport-related structural brain injury associated with an AC. The median age at presentation was 16 years (range 4–75 years). Headache was the most common presenting symptom (98%), followed by nausea and vomiting in 49%. Thirteen patients (21%) presented with a neurological deficit, most commonly hemiparesis. Open craniotomy was the most common form of treatment (49%). Bur holes and cyst fenestration were performed in 29 (45%) and 31 (48%) patients, respectively. Seven patients (11%) received a cystoperitoneal shunt. Four cases reported medical management only without any surgical intervention. No significant predictors were found for neurological deficit or open craniotomy. In the univariate model predicting the need for a cystoperitoneal shunt, the odds of receiving a shunt decreased as age increased (p = 0.004, OR 0.62 [95% CI 0.45–0.86]) and with male sex (p = 0.036, OR 0.15 [95% CI 0.03–0.88]).

CONCLUSIONS

This systematic review yielded 65 cases of sport-related structural brain injury associated with ACs. The majority of patients presented with chronic symptoms, and recovery was reported generally to be good. Although the review is subject to publication bias, the authors do not find at present that there is contraindication for patients with an AC to participate in sports, although parents and children should be counseled appropriately. Further studies are necessary to better evaluate AC characteristics that could pose a higher risk of adverse events after trauma.

ABBREVIATIONSAC = arachnoid cyst; ICP = intracranial pressure; IPH = intraparenchymal hemorrhage; IQR = interquartile range; PCS = postconcussion syndrome; SDH = subdural hematoma; SRC = sport-related concussion.

Abstract

OBJECTIVE

Arachnoid cysts (ACs) are congenital lesions bordered by an arachnoid membrane. Researchers have postulated that individuals with an AC demonstrate a higher rate of structural brain injury after trauma. Given the potential neurological consequences of a structural brain injury requiring neurosurgical intervention, the authors sought to perform a systematic review of sport-related structural-brain injury associated with ACs with a corresponding quantitative analysis.

METHODS

Titles and abstracts were searched systematically across the following databases: PubMed, Embase, CINAHL, and PsycINFO. The review was conducted in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement. Peer-reviewed case reports, case series, or observational studies that reported a structural brain injury due to a sport or recreational activity (hereafter referred to as sport-related) with an associated AC were included. Patients were excluded if they did not have an AC, suffered a concussion without structural brain injury, or sustained the injury during a non–sport-related activity (e.g., fall, motor vehicle collision). Descriptive statistical analysis and time to presentation data were summarized. Univariate logistic regression models to assess predictors of neurological deficit, open craniotomy, and cystoperitoneal shunt were completed.

RESULTS

After an initial search of 994 original articles, 52 studies were found that reported 65 cases of sport-related structural brain injury associated with an AC. The median age at presentation was 16 years (range 4–75 years). Headache was the most common presenting symptom (98%), followed by nausea and vomiting in 49%. Thirteen patients (21%) presented with a neurological deficit, most commonly hemiparesis. Open craniotomy was the most common form of treatment (49%). Bur holes and cyst fenestration were performed in 29 (45%) and 31 (48%) patients, respectively. Seven patients (11%) received a cystoperitoneal shunt. Four cases reported medical management only without any surgical intervention. No significant predictors were found for neurological deficit or open craniotomy. In the univariate model predicting the need for a cystoperitoneal shunt, the odds of receiving a shunt decreased as age increased (p = 0.004, OR 0.62 [95% CI 0.45–0.86]) and with male sex (p = 0.036, OR 0.15 [95% CI 0.03–0.88]).

CONCLUSIONS

This systematic review yielded 65 cases of sport-related structural brain injury associated with ACs. The majority of patients presented with chronic symptoms, and recovery was reported generally to be good. Although the review is subject to publication bias, the authors do not find at present that there is contraindication for patients with an AC to participate in sports, although parents and children should be counseled appropriately. Further studies are necessary to better evaluate AC characteristics that could pose a higher risk of adverse events after trauma.

Sport-related concussion (SRC) has emerged as a public health problem, affecting athletes of all ages and participation levels.11,35,43 While SRC by definition includes normal imaging results, a minority of sport-related head injuries result in structural brain injury.3,18,19,84,85 These cases are often neurosurgical emergencies and can result in permanent neurological deficit and/or death. Recent literature has postulated that athletes with arachnoid cysts (ACs) demonstrate a higher rate of structural brain injury after trauma, specifically subdural hematoma (SDH) or hygroma.37,44,79

ACs are congenital lesions bordered by an arachnoid membrane.37,49 Cysts are filled with CSF, occur in 0.7% to 1.7% of the general population,56,76 and are found most commonly on the left side with a 3:1 male to female predilection.37,78 Several reviews have discussed the risk of SDH or hygroma associated with ACs after head trauma.37,44,79 The underlying mechanism for these structural injuries is unknown, but theories propose that 1) vessels without support of the cyst wall are prone to rupture,17,66 2) vessels within the wall can rupture due to decreased compliance,55 or 3) a slit-valve mechanism is created, leading to increased pressure within the AC and vessel rupture.64 A select few reports have addressed the issue of return to sport with an AC, with or without structural injury.21,44

Given the uncertainty surrounding structural brain injuries in athletes with an AC and the experiences at our own neurosurgical department and sports concussion center, we sought to review the literature in this area. The goals of this systematic review were to identify all cases of sport-related structural-brain injury associated with ACs and to perform a quantitative analysis in this unique patient population. Both objectives represent an overarching goal to better characterize, prevent complications, and counsel about return to play in athletes with an AC.

Methods

Published titles and abstracts in the English language were searched systematically across the following electronic databases: PubMed, Embase, CINAHL, and PsycINFO. The search terms included MeSH terms and keywords. Search words included the following: arachnoid cyst, sport-related concussion, subdural hematoma, subdural hygroma, sports injuries, and athletic injuries. The Preferred Reporting Items for Systematic Reviews and Meta-Analyses45 were adapted to review a heterogeneous collection of literature. A flow diagram of the included studies is seen in Fig. 1. Example search syntax from PubMed is noted below:

FIG. 1.
FIG. 1.

Flow diagram representing systematic review process.

(“Arachnoid Cysts”[Mesh] OR arachnoid cysts[tiab] OR arachnoid cyst[tiab]) AND (“Hematoma, Subdural”[Mesh] OR subdural hematoma[tiab] OR subdural hemorrhage[tiab] OR “subarachnoid hemorrhage”[tiab] OR “Lymphangioma, Cystic”[Mesh] OR hygroma[tiab] OR hygromas[tiab] OR “Hydrocephalus”[Mesh] OR hydrocephalus[tiab] OR “Athletic Injuries”[Mesh] OR athletic injuries[tiab] OR sports injuries[tiab] OR recreational injuries[tiab] OR “sport”[tiab] OR “sports”[tiab] OR “athletics”[tiab] OR “Craniocerebral Trauma”[Mesh] OR “head trauma”[tiab] OR “brain injury”[tiab] OR “brain injuries”[tiab] OR “mild traumatic brain injury”[tiab] OR “mTBI”[tiab] OR “traumatic brain injury”[tiab] OR “tbi”[tiab] OR “injury”[tiab] OR “injuries”[tiab] OR “trauma”[tiab] OR “head injury”[tiab] OR “head injuries”[tiab] OR “concussion”[tiab] OR “concussions”[tiab] OR “complication”[tiab] OR “complications”[tiab])

Inclusion criteria consisted of the following: a case report, case series, or observational study of a patient with a structural brain injury due to a sport or recreational activity with an associated AC. Structural brain injury was defined most commonly as an acute or chronic SDH or subdural hygroma, in addition to less common injuries, such as epidural hematoma (EDH), subarachnoid hemorrhage (SAH), intraparenchymal hemorrhage (IPH), and skull fracture. “Sport-related” was defined according to definitions in earlier literature,84 specifically any endeavor in which an individual was performing an athletic activity alone or in competition against an opposing person or team. Patients were excluded if they did not have an AC, suffered a concussion without structural brain injury, or sustained the injury during a non–sport-related activity (e.g., fall, motor vehicle collision). While the question of whether patients with an AC are at increased risk of structural brain injury is an important one, incidence data cannot be calculate from the current systematic review. Rather, the question of whether athletes with an AC can return to play will be addressed.

After the initial search was completed, as described in Fig. 1, a separate review of all references of included studies was completed to ensure no cases were missed. All references of included studies were systematically reviewed. Of the 980 references from included papers, 169 full-text sources were searched for eligibility. All but 3 were excluded for the following reasons: unrelated (n = 97), unspecified or not a sport-related trauma (n = 8), or no trauma mentioned with AC complication (n = 61). The additional 3 sources were included in the final 52 articles.

Statistical Analysis

A descriptive statistical analysis was performed. Due to the limited sample size, a normal distribution was not assumed, and all data were considered to be nonparametric. Medians, interquartile ranges (IQR), and ranges were provided for continuous variables. Univariate logistic regression was performed to predict certain presentations or outcomes. A priori exposure variables included age, sex, days to presentation, presence of midline shift, and presence of a SDH. Multivariate analysis was not used due to limited sample and concern for an unstable model. Time to presentation data were represented with a Kaplan-Meier time to failure plot.29 All statistical analyses were performed in STATA (version 14, StataCorp LP).

Results

Our review yielded 52 studies reporting 65 cases of sport-related structural brain injury associated with an AC. The median year of publication was 2005, ranging from 1958 to 2015 (Fig. 2). The median age at presentation was 16 years (4–75 years) (Fig. 3), and 56 patients (86%) were male. Age was not mentioned in 2 studies, whereas sex was mentioned in all.

FIG. 2.
FIG. 2.

Histogram showing year of publication.

FIG. 3.
FIG. 3.

Kaplan-Meier failure plot of time from injury or symptom onset to discovery of structural abnormality.

Presentation

Presentation data are summarized in Table 1. The median time from either injury or symptom onset to discovery of the structural injury was 25 days, ranging from 1 to 168 days. Of all 65 patients, symptom endorsement was mentioned in 61 (94%) of studies. Headache was the most common symptom, presenting in all but 1 patient, followed by nausea and vomiting in 49%. Thirteen patients (21%) presented with a neurological deficit, most commonly hemiparesis. The range of sporting activities across all 52 studies is detailed in Table 2. Team sports were involved in 28 cases (43%).

TABLE 1.

Study and demographic variables

CharacteristicValue
Study type, no. (%)52 (100)
  Case report30 (58)
  Case series21 (40)
  Case-control1 (2)
Yr of publication, median (IQR)2005 (1997–2013)
Total cases, no. (%)65 (100)
  Pediatric41 (63)
  Adult24 (37)
Age in yrs, median (IQR)16 (12–21)
Male, no. (%)56 (86)
Time to presentation58 (100)
  Days to presentation, median (IQR)25 (10–35)
  Acute <7 days, n (%)9 (16)
  Chronic ≥7 days, n (%)49 (84)
Symptoms, no (%)61 (100)
  Headache60 (98)
  Nausea/vomiting30 (49)
  Dizziness6 (5)
  Diplopia8 (13)
  Other4 (7)
Neurological deficit, no. (%)61 (100)
  Extremity weakness4 (7)
  Numbness3 (5)
  Decreased responsiveness2 (3)
  CN VI palsy2 (3)
  Facial weakness2 (3)

CN = cranial nerve.

TABLE 2.

Sporting activities and cases in the 52 included studies

SportAuthors & YearNo. of Cases (%)*
SoccerOliver, 1958; Maeda et al., 1993; Kawanishi et al., 1999 (2 cases); Chillala et al., 2001; Prabhu & Bailes, 2002; Demetriades et al., 2004; Offiah et al., 2006; Domenicucci et al., 2009; Zeng et al., 2011; Işik et al., 2011; Maher et al., 2013; Edmondson et al., 2014; Takizawa et al., 201514 (22)
BicycleKulali & von Wild, 1989; Rogers et al., 1990; Donaldson et al., 2000; Pillai et al., 2009; Domenicucci et al., 2009; Seddighi et al., 2012; Blereau & Haley, 2013; Raveenthiran & Reshma 2014; Takizawa et al., 20159 (14)
FootballVigil et al., 1998; Donaldson et al., 2000; Gelabert-González et al., 2002; Bristol et al., 2007; Maher et al., 2013; Cress et al., 2013; Pascoe et al., 20157 (11)
Martial artsWeinberg & Flom, 1973; Yokoyama et al., 1989; Türkoğlu et al., 2008; Kertmen et al., 2012; Takizawa et al., 20155 (8)
Swimming/water sportsLaCour et al., 1978; Cullis & Gilroy, 1983; Rogers et al., 1990; Mori et al., 1995; Zhang et al., 20075 (8)
BasketballRogers et al., 1990; Tsuzuki et al., 2003; Chen et al., 2005; Hou et al., 20144 (6)
Physical/weight trainingOchi et al., 1996; Mori et al., 2002; Park et al., 20133 (5)
Ski/snowboardingTakizawa et al., 20152 (3)
BoxingRobles & Hernandez, 20061 (2)
CricketGupta et al., 20041 (2)
DancingMcNeil et al., 19871 (2)
EquestrianPage et al., 19871 (2)
HockeyEllis et al., 20151 (2)
RollerbladingAlbuquerque & Giannotta, 19971 (2)
RollercoasterHuang, 20031 (2)
RugbyVarma et al., 19811 (2)
SkateboardingVarma et al., 19811 (2)
VolleyballHamada et al., 20101 (2)
Sport not specifiedUlmer et al., 2002; Pretorius & McAuley, 2005; Tsitsopoulos et al., 2008; Zeng et al., 2011; Zheng et al., 2013 (2 cases)6 (8)
Total65

Due to rounding, total % is greater than 100%.

Denotes team sport.

Imaging and Treatment

Details regarding imaging and treatment are illustrated in Table 3. A CT scan and/or MRI of the head was obtained in all 65 cases. SDH was the most common structural injury (72%) followed by hygroma (23%), EDH (2%), and IPH (2%). The most common imaging finding of the structural abnormality (SDH or hygroma) on CT was an iso-/hypodense lesion signifying a chronic injury (76%). Consistent with prior literature, 75% of patients harbored left-sided ACs. Due to the heterogeneous terminology and lack of complete CT/MRI studies, middle fossa and sylvian locations were combined and represented 98% of cases. Skull thinning adjacent to the cyst was seen in 60% of cases and often mentioned as a clue for AC presence when visualization was difficult, most often in the case of intracystic hemorrhage or an emergent, life-saving situation.

TABLE 3.

Radiographic, treatment, and outcome variables

CharacteristicValue
Injury density, no. (%)54 (100)
  Hyperdense13 (24)
  Iso-/hypodense41 (76)
Side, no. (%)64 (100)
  Left48 (75)
  Right15 (23)
  Bilateral1 (2)
Location, no. (%)64 (100)
  Middle fossa/sylvian63 (98)
  Interhemispheric1 (2)
Skull thinning, no. (%)24/40 (60)
Structural Injury, no. (%)64 (100)
  SDH47 (73)
  Hygroma15 (23)
  EDH1 (2)
  IPH1 (2)
Midline shift, no. (%)39/49 (80)
Treatment, no. (%)65 (100)
  Bur hole26 (41)
  Open craniotomy29 (45)
  Bur hole & open craniotomy3 (5)
  Cyst fenestration31 (48)
  Cystoperitoneal shunt*7 (11)
  Surgery unspecified2 (3)
  No surgery4 (6)
Outcome mentioned, no. (%)36 (55)
Return to play mentioned, no. (%)4 (6)

Of note, 1 patient's only treatment was a cystoperitoneal shunt without bur hole or open craniotomy.

Four cases (6%) reported medical management only without any surgical intervention; in 1 of these cases the family was offered surgery but refused.6 Two cases were hygromas that were followed with serial imaging and were noted to decrease over time, and one was an isolated 2.3-cm IPH on the opposite side of the AC. Of the remaining 61 patients (94%), open craniotomy alone was performed in 29 patients (45%) and was the most common surgical procedure, followed by bur holes alone in 26 patients (41%); 3 patients (5%) underwent both. During the open craniotomy or bur hole, cyst fenestration was performed in 31 patients (48%). Seven patients (11%) received a cystoperitoneal shunt. Five patients (8%) underwent more than 1 operation. An endoscope was used in 2 cases (3%).24,75 A postoperative outcome was mentioned in 36 cases (55%). Each of the 65 cases is summarized in Table 4.

TABLE 4.

Itemized 65 cases

Case No.Authors & YearAge (yrs), SexSportPathologyMidline ShiftTreatmentOutcome
1Takizawa et al., 201513, MBicycleSDHNRBur holeNR
2Takizawa et al., 201531, MMartial artsSDHNRBur holeNR
3Takizawa et al., 201535, FSki/snowboardingSDHNRBur holeNR
4Takizawa et al., 201532, MSki/snowboardingSDHNROpen craniotomyNR
5Takizawa et al., 201515, MSoccerSDHNROpen craniotomyNR
6Pascoe et al., 201543, MFootballSDHYesOpen craniotomyNR
7Ellis et al., 201511, MHockeyIPHNoNo surgeryGood; no return to sport
8Raveenthiran & Reshma, 20144, MBicycleHygromaNoCystoperitoneal shuntGood
9Hou et al., 201417, MBasketballSDHYesBur holeGood
10Edmondson et al., 201414, MSoccerSDHYesBur holeGood
11Zheng et al., 201319, MNRSDHNRBur holeNR
12Zheng et al., 201316, MNRSDHNRBur holeNR
13Park et al., 201375, MPhysical/weight trainingSDHNoBur holeGood
14Maher et al., 201316, MFootballHygromaNoNo surgeryGood
15Maher et al., 201312, FSoccerHygromaNoNo surgeryGood
16Cress et al., 2013NR, MFootballSDH or hygromaNROpen craniotomyNR
17Blereau & Haley, 20137, FBicycleSDHYesBur hole; cystoperitoneal shuntGood
18Seddighi et al., 201223, MBicycleEDHYesOpen craniotomyNR
19Kertmen et al., 201212, MMartial artsSDHYesBur holeGood
20Zeng et al., 201116, MSoccerSDHYesBur holeGood
21Zeng et al., 201114, MNRSDHYesOpen craniotomyGood
22Işik et al., 201113, MSoccerSDHYesBur holeGood
23Hamada et al., 201015, MVolleyballSDHNoOpen craniotomyNR
24Pillai et al., 200923, MBicycleSDHYesBur hole; open craniotomyGood
25Domenicucci et al., 200941, MBicycleSDHNRBurr holeGood
26Domenicucci et al., 20097, MSoccerSDHNRBur holeGood
27Türkoğlu et al., 200825, MMartial artsSDHYesBur holeGood
28Tsitsopoulos et al., 200815, MNRSDHYesOpen craniotomyGood
29Zhang et al., 200721, MSwimming/water sportsSDHYesOpen craniotomyGood
30Bristol et al., 200717, MFootballHygromaNoOpen craniotomyGood
31Robles & Hernandez, 200620, MBoxingSDHYesOpen craniotomyGood
32Offiah et al., 20068, MSoccerHygromaYesOpen craniotomy; cystoperitoneal shuntGood
33Pretorius & McAuley, 200511, MNRSDHYesOpen craniotomyNR
34Chen et al., 200520, MBasketballSDHYesNo surgeryNR
35Demetriades et al., 200424, MSoccerSDHYesBur holeGood
36Gupta et al., 200422, MCricketHygromaNoBur holeNR
37Tsuzuki et al., 200316, FBasketballSDHYesBur holeGood
38Huang, 200333, FRollercoasterHygromaNoBur holeNR
39Ulmer et al., 200244, MNRSDHYesOpen craniotomyGood
40Prabhu & Bailes, 200216, FSoccerSDHYesOpen craniotomyNR
41Mori et al., 200214, MPhysical/weight trainingSDHYesBur holeGood
42Gelabert-González, 200213, MFootballHygromaYesOpen craniotomyGood
43Chillala et al., 200121, MSoccerSDHNoSurgery, unspecifiedGood
44Donaldson et al., 20005, MBicycleHygromaNRBur hole; open craniotomyGood
45Donaldson et al., 200014, MFootballHygromaNROpen craniotomyGood; returned to football
46Kawanishi et al., 199914, MSoccerSDHYesBur holeNR
47Kawanishi et al., 199911, MSoccerSDHYesBur holeNR
48Vigil et al., 199816, MFootballHygromaYesBur holeGood; returned to football
49Albuquerque & Giannotta, 19976, MRollerbladingHygromaYesOpen craniotomy; cystoperitoneal shuntGood
50Ochi et al., 199612, MPhysical/weight trainingSDHYesSurgery, unspecifiedNR
51Mori et al., 199529, MSwimming/water sportsSDHYesBur holeNR
52Maeda et al., 199314, MSoccerSDHYesOpen craniotomyNR
53Rogers et al., 199010, FBasketballSDHNRBur hole; cystoperitoneal shuntNR
54Rogers et al., 199011, MBicycleSDHNRBur holeNR
55Rogers et al., 199012, FSwimming/water sportsSDHNROpen craniotomy; cystoperitoneal shuntNR
56Kulali & von Wild, 1989NR, MBicycleHygromaYesOpen craniotomy; cystoperitoneal shuntNR
57Yokoyama et al., 198917, MMartial artsSDHYesOpen craniotomyNR
58Page et al., 198757, MEquestrianSDHYesOpen craniotomyNR
59McNeil et al., 198717, MDancingSDHYesOpen craniotomyGood; no return to dancing
60Cullis & Gilroy, 198311, MSwimming/water sportsHygromaYesOpen craniotomyNR
61Varma et al., 198117, MRugbySDHNROpen craniotomyGood
62Varma et al., 198113, MSkateboardingHygromaYesOpen craniotomyGood
63LaCour et al., 197813, FSwimming/water sportsSDHYesOpen craniotomyNR
64Weinberg & Flom, 197320, MMartial artsSDHYesBur hole; open craniotomyNR
65Oliver, 195821, MSoccerSDHYesOpen craniotomyGood

NR = not reported.

Three univariate models were conducted in an attempt to predict 1) a neurological deficit, 2) need for open craniotomy, and 3) need for a cystoperitoneal shunt (Table 5). The predictive factors in each model were determined a priori and included age, sex, days to presentation, midline shift, and presence of an SDH. No significant predictors were found for neurological deficit or open craniotomy. In the model predicting the need for a cystoperitoneal shunt, the odds of receiving a shunt decreased as age increased (p = 0.004, OR 0.62 [95% CI 0.45–0.86]) and with male sex (p = 0.036, OR 0.15 [95% CI 0.03–0.88]).

TABLE 5.

Univariate logistic regression analysis showing predictors of presentation and treatment

Predictive FactorOR95% CIp Value
Neurological deficit
  Age1.00(0.95–1.05)0.866
  Sex0.92(0.17–5.05)0.920
  Days to presentation0.99(0.97–1.02)0.608
  Midline shift1.09(0.19–6.19)0.926
  SDH1.33(0.20–2.30)0.532
Craniotomy
  Age1.00(0.96–1.04)0.819
  Sex2.42(0.55–10.70)0.245
  Days to presentation1.00(0.99–1.02)0.760
  Midline shift4.31(0.77–24.15)0.096
  SDH0.53(0.16–1.69)0.280
Cystoperitoneal shunt
  Age0.59(0.42–0.85)0.004
  Sex0.15(0.03–0.88)0.036
  Days to presentation0.97(0.90–1.04)0.321
  Midline shift0.97(0.09–9.90)0.979
  SDH0.25(0.05–1.28)0.096

Discussion

While posttraumatic SRC in general has been well studied, less is known about structural brain injuries in sports. ACs are congenital malformations with the potential to hemorrhage after relatively minor head injury. The goal of this systematic review was to summarize all cases of sport-related structural brain injury associated with ACs and to provide a quantitative analysis. A total of 65 cases were found across 52 studies, dating back to 1958. This review represents the largest of sport-related structural brain injury associated with ACs to date. The clinical implications of our findings are discussed below.

Presentation

An overwhelming majority of cases (84%) were chronic, with a median time to presentation of nearly 4 weeks. Many cases had multiple presentations to clinic for lingering symptoms, and only on the second or third visit was imaging performed. However, this trend is subject to publication bias, as a delayed SDH due to sports injury is more novel than the more common acute SDH. In addition, it is evident from our review that sport-related structural brain injury associated with ACs is not only a problem in team sports. Sporting activities ranged from martial arts to winter sports (e.g., skiing, snowboarding), and these nonteam sports accounted for the majority of cases. Furthermore, it is important to realize that athletes engaged in noncontact sports have also been reported to have AC hemorrhage, necessitating a high level of attention to patients regardless of the contact level of sport played.

How these patients present is perhaps most interesting when differentiating structural brain injury from post-concussion syndrome (PCS). PCS is a well-studied entity across many populations after general trauma, military blast injury, and SRC.25,39,67,69 Tator et al.69 comprehensively described the phenotype of PCS across 138 athletes, where most patients were younger than 30 years with an average of 7.6 symptoms for a median of 6 months. As both populations have symptom duration of weeks to months, differentiating between a recovering PCS patient with no structural injury versus one with an AC associated SDH or hygroma becomes challenging.

Based on our review, a persistent headache was present in 98% of patients, nausea and/or vomiting in nearly half, and diplopia in 13%. This symptom constellation represents a clear picture of increased intracranial pressure (ICP). In the previously mentioned study of PCS,69 headache was also endorsed by 90% of patients, followed by memory disorders (58%) and concentration problems (57%); nausea was endorsed by 37% of athletes and vomiting in only 3%. The issue of when to order imaging after SRC is a controversial one, as imaging in the chronic phase of PCS can be low yield and costly.16,46 However, imaging was potentially lifesaving in the reviewed population of 65 patients. Thus, based on the present systematic review, we recommend imaging when persistent signs and symptoms of increased ICP are present.32,36 Based on a median time to presentation of 25 days, imaging can be pursued at any time, but there may be a higher yield weeks after injury. Differentiating between symptoms of increased ICP versus PCS is much easier written than accomplished, but a detailed temporal history, fundoscopic examination checking for papilledema, and neuropsychological testing may aid in this differentiation. Furthermore, 13 patients (21%) presented with an objective neurological deficit such as hemiparesis or facial weakness, which is never seen in PCS. Imaging should promptly be performed in all patients who demonstrate a fixed neurological deficit on clinical examination.

Imaging and Treatment

Most structural injuries were seen as isodense or hypodense lesions, signifying the chronic nature of the subdural and/or intracystic hematoma. To our surprise, the AC location was difficult to standardize across many of the studies reviewed. The well-known Galassi classification quantifies ACs based on extent of middle fossa involvement and compression of adjacent neural structures.20 While some articles mentioned the Galassi type, most did not. Whereas some authors labeled an AC as middle fossa, others would call a similar lesion temporal. Thus, we were unable to delineate the AC location given the heterogeneous nomenclature used. We emphasize the need for future work of AC associated structural sport-related brain injury to standardize cyst location. Also, the size of the AC was not recorded in most studies, likely due to hemorrhage obscuring the ability to fully visualize the entire cyst. If possible, future studies should also include AC size details, as the relationship between AC size and hemorrhage is also unknown.

Open craniotomy was the most common mode of surgical treatment, and nearly half of all cases mentioned cyst fenestration. Fenestration to the basal cisterns was mentioned in select cases, with intraoperative visualization of the circle of Willis.57 Therefore, surgeons should be aware that complex dissections may be required in cases in which bur hole treatment alone is insufficient. Due to the paucity of outcomes, there are not enough data to recommend fenestration, but it certainly appears that in large enough ACs, fenestration should be done whenever possible. Moreover, an endoscope was used in 2 studies, which provides a reasonable, less invasive option.24,75 Another option for treatment that bears mention is acetazolamide to decrease CSF production, and in select cases has obviated the need for surgical treatment.8,38,41 Cystoperitoneal shunts were placed in 7 patients, and our model predicted that younger age was significantly associated with increased odds of a cystoperitoneal shunt placement, in addition to female sex.

In some cases, the AC was not realized until after the initial decompression, and a second operation was needed for definitive treatment.26,30,47 Though clearly evident in some cases, the cyst may be filled with acute or chronic blood products, making it difficult to see. Skull thinning was noted in 60% of cases, and can be a subtle, yet important finding when a SDH is seen after a sports injury or low energy trauma.

Future Directions

A more common problem than the case of a sport-related structural injury associated with ACs is the initial clinical discussion surrounding involvement in sports after the incidental finding of an asymptomatic AC.21 Unfortunately, minimal information is available in the literature to guide these decisions about sports participation with an AC. A postoperative outcome was mentioned in over half of the studies, often in a limited fashion, and all instances mentioned good or uneventful outcomes. Furthermore, only 3% of studies mentioned return to sport or activity. With the current estimate of asymptomatic ACs at 0.7%–1.7% of the population, it can be extrapolated that on an American football field comprising approximately 90 athletes from both teams, it would not be uncommon for at least 1 player to have an asymptomatic AC. The issue of involvement in sports with an AC, with or without structural injury, is an important one as surveillance imaging becomes increasingly used.

One report of a 32-year-old professional football player described an asymptomatic AC found on imaging for cervical radicular symptoms.21 The cyst was 7.5 cm in its greatest dimension and located in the left sylvian fissure. The player was cleared to play football and had no neurological sequelae, with normal findings on postseason MRI. Gamradt et al.21 postulated 2 questions: does the AC place the player at increased risk for a SDH or hygroma, and what are the sequelae of that structural injury? Anecdotally, the authors hypothesized the presence of an AC did confer a slightly higher risk of hemorrhage due to the cyst incompressibility and associated calvaria thinning, although the exact magnitude of the risk could not be quantified. Miele et al.44 echoed this sentiment, stating that although an AC may hold an increased risk of hemorrhage, it is not an absolute contraindication to participation in contact sports, and patients and family members should be counseled of these risks. Unfortunately, similar to other analyses, we cannot calculate incidence rates of hemorrhage, nor are we able to quantify risk.

To the second question, our systematic review yielded a somewhat incomplete answer. Of the 55% of studies that mentioned an outcome, all endorsed an uneventful recovery. However, most studies devoted only one sentence to the postoperative course. Thus, based on the limited information provided, we can say that in those studies that reported outcomes, all patients recovered well at the gross neurological level. According to the current evidence base, we do not feel that there is a clear contraindication for patients with an AC to participate in sports, although parents and children should be counseled of the perceived risks. Similar questions surround patients with Chiari malformations, which, when asymptomatic, have been viewed more as a relative than absolute contraindication.5,44 However, absolute contraindication is recommended in patients who are symptomatic, have brainstem compression, or harbor a syrinx.44 Although outside the scope of this systematic review, equally important are return to play issues in athletes with a ventriculoperitoneal shunt, epilepsy, or prior craniotomy.44

Limitations

Although our study represents a comprehensive review, biases of a retrospective review exist. First, publication bias may be present in 3 major forms: the predilection to publish on 1) good outcomes, 2) patients who underwent surgery, and 3) patients with delayed clinical findings. The push for publication may be a reason that all but 3 of the 52 studies reviewed described operative treatment, when in reality nonoperative treatment may occur more commonly than is presented. Furthermore, delayed (as opposed to acute) clinical findings are more likely to be published, as these tend to be more novel and reportable. Second, sport-specific data were sparse, and in some studies only a remote history of sport was mentioned, sometimes without a distinct impact or collision. Several studies reported unspecified athletic events, which could represent a wide range of sporting activities. Thus, we had to rely on the limited history provided. Third, operative details were not recorded uniformly across authors, and some studies lacked important detail in dictating operative treatment.

Conclusions

Sport-related structural brain injury associated with an AC is a rare occurrence. The current systematic review informs us that these injuries are often chronic, with median time to presentation of 25 days, and most commonly presenting with headache and nausea/vomiting. Injuries occur in both team/nonteam and contact/noncontact sports, and the majority are treated with open craniotomy or bur hole. Outcomes were good in all studies that mentioned one.

That said, substantial information is needed to better treat and avoid these serious injuries. Cyst location was not standardized in most studies, nor was cyst size mentioned, making the relationship between cyst size and risk of rupture impossible to ascertain. Furthermore, significant gaps in postoperative outcomes and return to sport were found. According to the current evidence base, we do not feel that there is a clear contraindication to participate in sports in patients with an AC, although parents and children should be counseled appropriately. Further studies are necessary to better evaluate AC characteristics that could pose a higher risk of adverse events after trauma.

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Disclosures

The authors report the following. Dr. Solomon receives consulting fees from the Tennessee Titans (NFL), the Nashville Predators (NHL), and the athletic departments for several universities. In addition he is a member of the ImPACT advisory board and receives reimbursement for expenses to board meetings, and also receives royalties from book sales. Dr. Sills is a consulting physician to the Nashville Predators (uncompensated) and also serves as an unaffiliated neurotrauma consultant for the NFL. Dr. Bonfield serves as an unaffiliated neurotrauma consultant for the NFL.

Author Contributions

Conception and design: Zuckerman, Solomon, Sills, Bonfield. Acquisition of data: Prather, Yengo-Kahn. Analysis and interpretation of data: all authors. Drafting the article: Zuckerman. Critically revising the article: all authors. Reviewed submitted version of manuscript: Zuckerman, Solomon, Sills, Bonfield. Approved the final version of the manuscript on behalf of all authors: Zuckerman. Statistical analysis: Zuckerman. Administrative/technical/material support: Solomon, Sills, Bonfield. Study supervision: Solomon, Sills, Bonfield.

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Article Information

INCLUDE WHEN CITING DOI: 10.3171/2016.1.FOCUS15608.

Correspondence Scott L. Zuckerman, Department of Neurological Surgery, Vanderbilt University School of Medicine, 1211 Medical Center Dr., Medical Center North T-4224, Nashville, TN 37212. email: scott.zuckerman@vanderbilt.edu.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Flow diagram representing systematic review process.

  • View in gallery

    Histogram showing year of publication.

  • View in gallery

    Kaplan-Meier failure plot of time from injury or symptom onset to discovery of structural abnormality.

References

1

Albuquerque FCGiannotta SL: Arachnoid cyst rupture producing subdural hygroma and intracranial hypertension: case reports. Neurosurgery 41:9519561997

2

Blereau RPHaley TJ: Arachnoid cyst. Consultant 53:5405412013

3

Boden BPTacchetti RLCantu RCKnowles SBMueller FO: Catastrophic head injuries in high school and college football players. Am J Sports Med 35:107510812007

4

Bristol REAlbuquerque FCMcDougall CSpetzler RF: Arachnoid cysts: spontaneous resolution distinct from traumatic rupture. Case report. Neurosurg Focus 22:2E22007

5

Callaway GHO'Brien SJTehrany AM: Chiari I malformation and spinal cord injury: cause for concern in contact athletes?. Med Sci Sports Exerc 28:121812201996

6

Chen HYLi YSChen CHShen WCYing KS: Concomitant traumatic spinal hematoma and hemorrhage from intracranial arachnoid cyst following minor injury. Zhonghua Fang She Xue Za Zhi 30:1731772005

7

Chillala SRead CEvans PA: An unusual case of subdural haematoma presenting to the accident and emergency department. Emerg Med J 18:3083092001

8

Choong CTLee SH: Subdural hygroma in association with middle fossa arachnoid cyst: acetazolamide therapy. Brain Dev 20:3193221998

9

Cress MKestle JRHolubkov RRiva-Cambrin J: Risk factors for pediatric arachnoid cyst rupture/hemorrhage: a case-control study. Neurosurgery 72:7167222013

10

Cullis PAGilroy J: Arachnoid cyst with rupture into the subdural space. J Neurol Neurosurg Psychiatry 46:4544561983

11

Daneshvar DHNowinski CJMcKee ACCantu RC: The epidemiology of sport-related concussion. Clin Sports Med 30:117vii2011

12

Demetriades AKMcEvoy AWKitchen ND: Subdural haematoma associated with an arachnoid cyst after repetitive minor heading injury in ball games. Br J Sports Med 38:E82004

13

Domenicucci MRusso NGiugni EPierallini A: Relationship between supratentorial arachnoid cyst and chronic subdural hematoma: neuroradiological evidence and surgical treatment. J Neurosurg 110:125012552009

14

Donaldson JWEdwards-Brown MLuerssen TG: Arachnoid cyst rupture with concurrent subdural hygroma. Pediatr Neurosurg 32:1371392000

15

Edmondson LUpshaw JETuuri RE: A 14-year-old male with a 10-week history of headaches. Pediatr Ann 43:2202222232014

16

Ellis MJLeiter JHall TMcDonald PJSawyer SSilver N: Neuroimaging findings in pediatric sports-related concussion. J Neurosurg Pediatr 16:2412472015

17

Eustace SToland JStack J: CT and MRI of arachnoid cyst with complicating intracystic and subdural haemorrhage. J Comput Assist Tomogr 16:9959971992

18

Forbes JAZuckerman SAbla AAMocco JBode KEads T: Biomechanics of subdural hemorrhage in American football: review of the literature in response to rise in incidence. Childs Nerv Syst 30:1972032014

19

Forbes JAZuckerman SLHe LMcCalley ELee YMSolomon GS: Subdural hemorrhage in two high-school football players: post-injury helmet testing. Pediatr Neurosurg 49:43492013

20

Galassi ETognetti FGaist GFagioli LFrank FFrank G: CT scan and metrizamide CT cisternography in arachnoid cysts of the middle cranial fossa: classification and patho-physiological aspects. Surg Neurol 17:3633691982

21

Gamradt SCBrophy RBarnes RBirchansky SRodeo SAWarren RF: Incidental findings in cerebral imaging: arachnoid cyst in a professional football player. Clin J Sport Med 18:97992008

22

Gelabert-González MFernández-Villa JCutrín-Prieto JGarcìa Allut AMartínez-Rumbo R: Arachnoid cyst rupture with subdural hygroma: report of three cases and literature review. Childs Nerv Syst 18:6096132002

23

Gupta RVaishya SMehta VS: Arachnoid cyst presenting as subdural hygroma. J Clin Neurosci 11:3173182004

24

Hamada HHayashi NUmemura KKurosaki KEndo S: Middle cranial fossa arachnoid cyst presenting with subdural effusion and endoscopic detection of tear of the cyst—case report. Neurol Med Chir (Tokyo) 50:5125142010

25

Harch PGAndrews SRFogarty EFAmen DPezzullo JCLucarini J: A phase I study of low-pressure hyperbaric oxygen therapy for blast-induced post-concussion syndrome and post-traumatic stress disorder. J Neurotrauma 29:1681852012

26

Hou KLi CGZhang YZhu BX: The surgical treatment of three young chronic subdural hematoma patients with different causes. J Korean Neurosurg Soc 55:2182212014

27

Huang PP: Roller coaster headaches revisited. Surg Neurol 60:3984012003

28

Işik HSYildiz ÖCeylan Y: Chronic subdural hematoma caused by soccer ball trauma associated with arachnoid cyst in childhood: Case report. J Neurol Sci (Turk) 28:3984012011

29

Kaplan ELMeier P: Nonparametric estimation from incomplete observations. J Am Stat Assoc 53:4574811958

30

Kawanishi ANakayama MKadota K: Heading injury precipitating subdural hematoma associated with arachnoid cysts—two case reports. Neurol Med Chir (Tokyo) 39:2312331999

31

Kertmen HGürer BYilmaz ERSekerci Z: Chronic subdural hematoma associated with an arachnoid cyst in a juvenile taekwondo athlete: a case report and review of the literature. Pediatr Neurosurg 48:55582012

32

Kontos APElbin RJSchatz PCovassin THenry LPardini J: A revised factor structure for the post-concussion symptom scale: baseline and postconcussion factors. Am J Sports Med 40:237523842012

33

Kulali Avon Wild K: Post-traumatic subdural hygroma as a complication of arachnoid cysts of the middle fossa. Neurosurg Rev 12:Suppl 15085131989

34

LaCour FTrevor RCarey M: Arachnoid cyst and associated subdural hematoma. Observations on conventional roentgenographic and computerized tomographic diagnosis. Arch Neurol 35:84891978

35

Langlois JARutland-Brown WWald MM: The epidemiology and impact of traumatic brain injury: a brief overview. J Head Trauma Rehabil 21:3753782006

36

Lau BCCollins MWLovell MR: Cutoff scores in neurocognitive testing and symptom clusters that predict protracted recovery from concussions in high school athletes. Neurosurgery 70:3713792012

37

Liu ZXu PLi QLiu HChen NXu J: Arachnoid cysts with subdural hematoma or intracystic hemorrhage in children. Pediatr Emerg Care 30:3453512014

38

Longatti PMarton EBilleci D: Acetazolamide and corticosteroid therapy in complicated arachnoid cyst. Childs Nerv Syst 21:106110642005

39

Lynch JMAnderson MBenton BGreen SS: The gaming of concussions: a unique intervention in postconcussion syndrome. J Athl Train 50:2702762015

40

Maeda MKawamura YHanda YKubota TIshii Y: Value of MR imaging in middle fossa arachnoid cyst with intracystic and subdural hematoma. Eur J Radiol 17:1451471993

41

Maher COGarton HJAl-Holou WNTrobe JDMuraszko KMJackson EM: Management of subdural hygromas associated with arachnoid cysts. J Neurosurg Pediatr 12:4344432013

42

McNeil SLSpruill WALangley RLShuping JRLeonard JR III: Multiple subdural hematomas associated with break-dancing. Ann Emerg Med 16:1141161987

43

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