Prevalence of Subdural Collections in Children with Macrocrania

Discussion

Previous reports state that the most common cause of subdural hemorrhage in children is AHT.^17,24 The finding of unexplained SDC in a young child should initiate consideration of AHT; however, this must be closely correlated with the clinical context, other imaging, and laboratory findings. Bleeding diatheses, various genetic conditions (eg, glutaric aciduria type I), overshunting, and rapid decreases in brain volume have been associated with SDC in children after minimal or no trauma^3,16,25 and should be kept in mind when evaluating these patients.

Enlarged SS have been described in association with SDC in children by several authors and have been implicated as a predisposing cause.^{7,9⇓–11,20,26⇓⇓⇓⇓–31} Variable methodology, cohort makeup, clinical assessments for AHT, and imaging techniques in these studies make conclusions regarding SDC etiology difficult.

SDC in children can have a wide range of appearances, depending on etiology, imaging test used, and age of the collection.^12,14,16 “Subdural hematoma” has been used very loosely in the literature in this population and probably has described a wide range of SDC with different etiologies, including “subdural hygroma,”²⁵ “chronic subdural hematoma,”¹⁶ “chronic subdural hematoma with rebleeding,”¹² and “hemato-hygroma.”¹⁴ In clinical practice, it is often difficult to differentiate these, adding to the complexity in evaluating these children.^12,25 For this reason, we chose to use the nonetiologic term “subdural collections” in our study to describe these collections.

Five previous studies have described SDC in populations of children with enlarged SS with prevalence estimates between 8–23% in series with between 20–142 subjects. The largest of these studies described a mixed group of children with enlarged extra-axial spaces on head sonography.³⁰ They found 33 SDC in 142 subjects over a 4-year period. Twenty-five were anechoic (CSF-like) and 8 were echogenic or complex; 103 of these subjects had macrocrania, though the presence of macrocrania and enlarged spaces was not correlated with SDC visualization. Although children with prior major hemorrhage were excluded, children with prior meningitic effusions, white matter injury of prematurity, and “malformative syndromes” were included in their cohort, limiting conclusions. Few subjects had CT imaging, limiting detection of acute hemorrhage. Of the children with SDC, 4 cases were “battered children”; however, AHT evaluation details are limited. Azais and Echenne²⁹ describe 5 SDC in 41 children with “benign enlargement of the SS” identified primarily with sonography, 29 (72%) of whom had macrocrania. They excluded children with prematurity, intrauterine growth restriction, malnutrition, and neonatal distress. Three SDC were “unexpected” and not associated with any reported trauma. One was related to accidental trauma and 1 was related to probable AHT. Hellbusch²⁶ described 9 SDC in 47 highly selected children referred for neurosurgical evaluation of enlarged extra-axial spaces. Traumatic cases (both accidental and AHT) were excluded, and no detailed description of imaging findings was reported.

Three recent studies specifically evaluated SDC in children with enlarged extra-axial spaces.^10,11,32 However, because the cases were identified on the basis of the presence of SDC, no inference as to the true prevalence of SDC in the overall group with enlarged extra-axial spaces is possible. Ghosh and Ghosh¹⁰ described 9 patients (3 months to 2 years of age) with SDH and enlarged extra-axial spaces identified by searching for the ICD-9 diagnoses of “nontraumatic SDH” and “hydrocephalus” over a 10-year period. They excluded patients with true hydrocephalus, shunts, head injury, and cerebral atrophy. The identified collections were bilateral in 6 and exhibited a wide range of imaging appearances. All were evaluated for AHT, but only 1 subject was reported to children's services. McNeely et al¹¹ described 7 children with SDC and enlarged SS identified in a nonspecified manner in a 6-year period. Children with known AHT and bleeding diatheses were excluded. Collections were bilateral in 3. One was involved in a major motor vehicle collision and 1 had a reported fall with skull fracture. The others were identified on imaging performed for macrocrania or lethargy, and no other etiology was identified. Vinchon et al³² described 16 children with “spontaneous” SDH (no traumatic history, bleeding disorder, or AHT) identified from a prospective neurosurgical data base; 12 had enlarged SS, and 12 had macrocrania. They compared patients with spontaneous SDH with a group with AHT or accidental trauma and found that the children with spontaneous SDH were much more commonly macrocephalic (75% versus 20%).

Although the published associations between enlarged SS and SDC as well as data from our study suggest a link, documented spontaneous SDC in children with enlarged SS and prior imaging without SDC, are rare. We could find only 12 previously reported spontaneous, nontraumatic SDC in children with prior imaging documentation.^{7,20,26,31⇓–33} The best documented of these reports is from Amodio et al,²⁰ who described a 3.5-month-old, former 32-week preterm boy, with grade 1 germinal matrix hemorrhage presenting with macrocrania. Initial head ultrasound examination demonstrated enlarged extra-axial spaces but no SDC. With continuing HC increase, a 6-week follow-up head ultrasound examination was performed that demonstrated new bilateral SDC containing low-level echoes. A subsequent MRI demonstrated large bilateral SDC with layering hemorrhagic material, confirmed at surgical drainage. Evaluation for AHT (including skeletal survey and retinal examination) was negative. In evaluating the images in this report, marked diffuse subarachnoid space enlargement is noted, however, suggesting brain volume loss. In our study, 4 patients with SDC had previous imaging (ultrasound examination, 3; CT, 1). In 3 patients, SDC were not identified on prior imaging, though the size of the identified SDC probably would have been too small to visualize on the imaging test performed (ultrasound examination and CT). In 1 case, retrospective assessment of a prior head ultrasound examination documented small SDC, not mentioned on the clinical report.

Data from the current study and the limited literature do support that SDC may arise in children with enlarged SS, after minimal or no trauma. The exact etiology is incompletely understood. However, some theories have been postulated.^12,14 Enlargement of the subarachnoid space may stretch and place increased strain on bridging veins, with resultant rupture and SDH formation.^7,13,29 This potential increased strain on bridging veins has been modeled mathematically¹³ but is not universally accepted.³⁴ Membranes surrounding an aging subdural hematoma are highly vascularized and have been postulated to potentially allow rebleeding either spontaneously or with minimal trauma.^12,35,36 A rent in the arachnoid could occur, allowing communication of the subdural and SS and subsequent subdural CSF collections to form.¹⁴

Although numbers are small and the clinical child abuse directed assessment was not performed on all patients, our report suggests small homogeneous SDC on cross-sectional imaging, without definite evidence of hemorrhage, may occur in the setting of BESS and may not indicate inflicted injury. In our study, 2 of the 6 children with SDC had findings suggesting child abuse. Both of these subjects had moderate-sized, bilateral, heterogeneous collections. The remaining 4 patients had radiographically similar SDC that were small, homogeneous, and localized over the convexities. Heterogeneous, more complex collections, particularly with clear evidence of hemorrhage by CT or MRI, could represent an important finding that suggests inflicted injury in the appropriate clinical scenario.

Only a few of the previous studies of SDC in children with enlarged SS report documentation of a dedicated evaluation of AHT.^7,8,10,20 In these studies, a total of 14 cases of SDC in the setting of enlarged SS have been described. All were investigated, but only 1 was thought to be related to AHT. Although imaging findings are incompletely described, 1 controversial case report describes a small “acute” SDH in a 4-month-old boy with macrocrania and enlarged extra-axial spaces who fell from a standing position to a carpeted floor.⁸ CT images were not presented in the report; however, MR images document small mixed intensity SDC. Although these studies document SDC in children after minimal or no trauma, they are all limited to varying degrees by incomplete description of imaging findings, variability in clinical assessment of potential abuse, and selection bias.

Age and sex differences were noted between subgroups of patients in our study. A male predominance in both the overall group of patients with macrocrania and those with enlarged SS was noted, consistent with prior studies.² Subjects with macrocrania and enlarged SS were younger than those subjects with normal SS, a finding described in other studies of BESS.² Enlarged SS typically normalize by 2–3 years of age in BESS.^2,22,37 The patients with macrocrania and normal SS in our study may be at the later stages of this condition.

There are some limitations to this study. Although all subjects had enlarged HC and many (61%) had enlarged SS, how many of this group fulfilled the full clinical scenario of “benign enlargement of the subarachnoid spaces” is unknown. Given our extensive exclusionary process, most subjects with macrocrania and enlarged SS probably did fit the criteria for BESS. Evaluation of subarachnoid space size was subjective for categorization in our study but did rely on the assessments of at least 2 radiologists. Our subjective assessment was subsequently validated by a quantitative analysis. Prior studies of normative subarachnoid space size in children are few; however, findings on cross-sectional imaging and ultrasound examination^23,38 correlate well with the results of our study. No sampling of the SDC was performed to assess the etiology of the collections. In 1 case, there was definite imaging evidence of hemorrhage. In the other cases, no hemorrhage could be documented and the collection contents remain unknown.

Those cases in which sonography provided the only evaluation were excluded, which potentially introduced selection bias. It is possible that those evaluated by cross-sectional imaging may be a different clinical group, with more concern regarding neurologic function, than those evaluated only by sonography. Although sonography can identify large SDC, its sensitivity for smaller collections is limited compared with CT/MRI. We chose not to include this group for the purposes of this study. MRI is the most sensitive test for SDC in this population,²¹ and small SDC could have been missed in subjects who only had CT imaging. Of the identified SDC in our study, 2 were initially identified by CT, with subsequent confirmation by MRI. The remaining subjects were identified by MRI. A study using only MRI for evaluation would be expected to identify a larger number of SDC. Further prospective studies should consider the use of MRI for evaluation in this cohort. Not all children with SDC received a dedicated clinical assessment for child abuse, limiting the ability to draw definite conclusions on the basis of imaging appearance of the collections. The appearance of some of the collections on imaging (large, complex, and clearly hemorrhagic) probably introduced bias for investigation of potential AHT in these subjects. It is possible that some of the other children with SDC identified in this study were, in fact, victims of child abuse. On the basis of clinical and imaging follow-up available, we believe that this is unlikely.