Frequency of macroscopic intradural hemorrhage with and without subdural hemorrhage in early childhood autopsies

It has been suggested that intradural hemorrhage is relatively common in the perinatal, neonatal, infant, and early childhood age groups, including in alleged cases of abusive head trauma (AHT) [ 1, 2]. It is particularly prevalent in the falx and tentorium [ 3].

Subdural hemorrhage is often seen in cases of AHT, with the most commonly suggested source of hemorrhage being traumatic damage to blood vessels, known as bridging veins, which traverse from the surface of the brain to the dural membrane. However, over the last two decades, alternative theories have emerged which suggest that infantile subdural bleeding may result from hypoxia, brain swelling and raised central venous pressure [ 1] and that the source of blood leakage is arterial and venous plexuses within the dura itself [ 3]. These theories, therefore, suggest that an intradural hemorrhage (IDH) occurs, subsequently producing a SDH via leakage out of the dura [ 4].

For IDH to result in SDH that is macroscopically visible at post-mortem, one might expect that the area of bleeding within the dura would need to be extensive enough to diffuse out of the membrane, into the subdural compartment, as proposed.

Our previous development of novel post-mortem techniques to remove the infant calvarial bones without damage to the dura [ 5] and careful dissection of the brain (including separate hemispherectomy) has allowed us to carefully document bridging veins and subdural bleeds [ 6]. The use of hemispherectomy and a standardized approach to photography of the brain and dura for these purposes created an archive of photos of the falx and tentorium in situ in a series of pediatric cases. Using our detailed dissection methods, we did not feel that macroscopically significant IDH was a common observation, in contrast to observations made in previous publications, particularly in the infant and young child age groups.

In this paper, we describe the occurrence of macroscopically visible intra-falcine and intra-tentorial hemorrhages, observed by two consultant forensic pathologists, in a series of photographs from 27 neonatal, infant and early childhood post-mortem examinations. We also describe several cases with documented SDH, to help elucidate whether or not the previously suggested link between IDH and SDH was evident in our study cohort.

The occurrence of IDH has previously been reported from autopsy photographs, post-mortem reports and histological examination of the falx and tentorium in a retrospective study [ 2]. In this current study, a substantial level of agreement was calculated between the two experienced observing forensic pathologists, using the same images and viewing conditions and with similar levels of experience and training. Whilst this kappa value (0.669) is a good level of agreement it is important to bear in mind that any agreement less than perfect (1.0) is a measure not only of agreement, but also the reverse, disagreement amongst the observers [ 8]. Therefore, the value in this study of less than 1.0 demonstrates the occurrence of cases in which the observers did not agree on the presence/absence of IDH. It has been suggested that when used for health research questions, judgements about what level of kappa should be classed as acceptable need to be made. The author of one paper has suggested an alternative interpretation of kappa in which 0.60–0.79 shows moderate agreement and 0.80–0.90 shows a strong agreement [ 8].

The method described in our previous publication [ 6] of removing each hemisphere separately provides the opportunity to observe and photographically document the falx and tentorium, in situ, including the presence of both macroscopically visible SDH and IDH. Providing access to clinical data and a previous pathologist’s interpretation of autopsy findings may influence analysis of autopsy images, and for this reason Pathologist A and B were blinded to all case histories.

Our study is congruent with the findings of previous papers [ 1, 3] in which IDH is more commonly seen in the younger age groups, with 7/10 of our cases with agreed IDH occurring in the neonatal group, 5 of which were ≤ 3 days old. This demonstration of IDH in this period, not long after birth, may indicate a susceptibly for IDH in this age group due to the birth, which in itself is not an atraumatic process (including potential molding of the bones due to compression) and may sometimes also require intervention such as forceps or ventouse delivery.

In an earlier combined macroscopic and histological study of dural samples taken from 55 fetuses and neonates with obvious macroscopic IDH, it was recorded that the majority of IDHs presented as diffuse in both the falx and tentorium [ 3]. This study also described a thin film SDH over the convexities in 16/25 (64%) fetuses and 20/30 (66.7%) neonates. Diffuse intra-falcine hemorrhage was recorded for all fetal cases with SDH and in 17/19 (89.5%) neonates in which SDH was documented (the 20th neonatal case with SDH did not have the dura examined for IDH).

A further study by the same group detailing an audit of post-mortem reports (including histology of dura) and photographs from two NHS hospitals [ 2] reported 55 cases of fetal SDH and 72 cases of infant and child SDH, all of which had IDH. One can deduce from the published results section and tables that all IDH were classified as ‘macroscopic’ when associated with SDH. Investigation of the 27 cases presented in our study, showed that there were 8 cases of SDH at autopsy. Of these 8, Pathologist A and B agreed on the presence of diffuse IDH in 3 cases, focal IDH in 1 case and no IDH in 3 cases. In the remaining case Pathologist A observed focal IDH and Pathologist B was unable to make an observation from the photographs. Therefore, our data does not support a direct and consistent correlation between the macroscopic presence and extent of IDH and SDH. We recognize that our small study cohort limits statistical analysis and that future investigation of a larger group would be necessary to confirm the results presented in this paper.

Accurate and consistent reporting of the macroscopic presence of IDH from autopsy photographs can be compromised due to potential SDH obscuring sections of the dura in some cases and also the differentiation between very small amounts smears of blood occurring within the dura itself or on the surface of the membrane (and in fact SDH). This may be a particular problem when viewing the falx after an initial post-mortem right hemispherectomy as SDH behind the dura, within the inter-hemispheric fissure, could potentially be mistaken for IDH. The assessment of IDH is further complicated by the presence of the blood-filled sinuses within the dura which could potentially be mistaken for IDH. For these reasons, we instructed pathologists to view both right and left aspects of the falx (after removal of both hemispheres) to make a more informed assessment. When intradural hemorrhage was present, it often appeared close to the dural venous sinuses, particularly the straight and superior sagittal sinuses (Fig. 2d). Histological examination of the tissue would be necessary to provide evidence that the blood was within the dura and not in the sinuses or one of the lesser documented smaller venous sinuses (sometimes referred to as meningeal veins or lakes) [ 9– 11]. We did not take samples of dura for histological examination in all of our cases as this is not our routine autopsy practice when there is no macroscopically visible SDH, dural tear, or extensive IDH. However, histological examination of apparent macroscopic IDH could be considered in prospective research cases to confirm the presence and exact location of bleeding, in which the appropriate consent and ethical approvals could be obtained.

In summary, our findings in this study have highlighted a substantial level of agreement for the retrospective interpretation of post-mortem photographic images for the purpose of detection of macroscopic IDH. We have also identified a much lower frequency of macroscopically identifiable IDH occurring alongside SDH than that which has previously been described in studies which also used histology in their assessment [ 2, 3].