High prevalence of non-accidental trauma among deceased children presenting at Level I trauma centers in the Netherlands

In 2003, the United Nations Children’s Fund reported that at least 3,500 children residing in high-income countries die annually as a result of non-accidental injuries (NAI) [1]. The prevalence of child abuse in the Netherlands has been estimated to be between 90,000 – 127,000 cases annually [2, 3]. According to Statistics Netherlands, there are approximately 3.4 million children currently living in the Netherlands [4] and 1,000–1,100 child deaths each year [5].

From 1996 to 2009, 445 cases of childhood death were referred to the Netherlands Forensic Institute (NFI) for mandatory autopsies; 239 of these children died due to NAI [6], corresponding to an average of 17 cases of fatal NAI per year. However, this is likely to be an underestimation resulting from selection bias. Some cases that were categorized as natural death might have been recognized as unnatural death due to NAI if a full postmortem investigation had been performed. Article 2 of the Council of Europe Committee of Ministers (CECM) statement on the harmonization of rules governing medicolegal autopsies states clearly that autopsies should be carried out in all cases of obvious or suspected unnatural death in both children and adults [7, 8]. While recommendations suggest that these principles should be implemented by all member states of the European Union, adoption of the entire set of guidelines is not currently mandatory. Moreover, member states are permitted to design their own systems based on these guidelines. Article 2 of the CECM has not been ratified in the Netherlands. The system currently in place in the Netherlands focuses on the results of a complete physical examination of the deceased; postmortem radiological imaging studies or legally mandated autopsies are only performed if there are suggestions or strong indications that death was a result of a criminal act. In contrast to cases of adult deaths, a forensic physician must be consulted in all pediatric deaths before a certificate of death can be issued. A consultation can result in one of three possible scenarios (Fig. 1). In the first scenario, there will be a clear indication of an unnatural cause of death, a situation that may lead to a full medicolegal evaluation. The second scenario addresses an expected, i.e., natural cause of death, for example, death of a child in palliative care due to the progression of a metastatic tumor. In this case, the body is released to the caregivers. The third scenario addresses cases in which the cause of death remains unclear. In these cases, a non-mandatory postmortem evaluation (as per the “Nader Onderzoek naar de DoodsOorzaak van Kinderen” [NODOK] or “Further Examination of the Cause of Death in Children” procedure) is offered to the caregivers [9‐11].

Between 0.1–3% of injured children admitted to the Emergency Department (ED) ultimately die as a result of their injuries (i.e., experience an unnatural death) [12, 13]. After consultation with the attending physician, the forensic physician will discuss the events leading to the presentation at the ED and the findings of the postmortem physical examination with the district attorney (DA). The decision as to whether the body can be released to the caregivers or taken into custody for a legally mandated autopsy lies solely with the DA. All legally mandated autopsies will be performed at the Netherlands Forensic Institute (NFI). The decision is based primarily on whether a given death was the result of a criminal act. In other words, postmortem investigations in unnatural deaths identified in the Netherlands are primarily initiated to rule out a crime, rather than to explain the cause of death.

Despite required consultations with forensic physicians, the prevalence of non-accidental death remains unclear. Equally important, the characteristics of fatal NAI in children have not been fully identified.

This study aimed to answer the following research questions:

(1) What is the prevalence of non-accidental trauma (NAT) in children who were admitted to and died at Level I trauma centers (TCs) in the Netherlands?

(2) What are clinical and postmortem features of non-accidental and accidental death in children who were admitted to these Level I TCs?

We report here the 20% prevalence of fatal NAT among children admitted to a Level I TC. We showed that 9.7% of the cases succumbed to inflicted trauma and 10.3% to the consequences of neglect. Fatal NAT was identified significantly more frequently as the cause of death in preschool-aged children (< 5 years old) compared to children in the older age cohorts. Subgroup analysis in young children (< 2 years old) revealed a 37% prevalence of inflicted trauma and a 6% prevalence of neglect.

One important finding relates to the cause of inflicted deaths. Of the cases of inflicted trauma, 64% presented to the ED as “sudden cardiopulmonary arrest”. This finding has extremely important implications, as there may be cases of non-accidental cases of inflicted trauma presenting as “sudden death” that have not been evaluated appropriately. Consequently, cases of non-accidental inflicted trauma may have been ignored because not all cases of sudden death undergo postmortem investigations. Although the NODOK procedure is offered to caregivers, none of these investigations are mandatory. Autopsies are rejected by caregivers in three of ten cases. These findings might be considered in light of another recent study from the Netherlands in which 85% of NODOK cases underwent an autopsy [11]. The limited frequency of autopsies may lead to a misdiagnosis of sudden infant death syndrome (SIDS), or sudden unexpected death in infancy (SUDI) [21, 22]. A small fraction of reported SIDS/SUDI cases may be covert NAI; of note, the distribution of SIDS has remained stable over the years while preventive measurements have been drastically improved [23, 24]. For example, Cote et al. [25] reported that 2.6% of 623 deaths attributed to SIDS were actually due to NAI. They also note that the proportion of non-SIDS deaths was significantly higher (18% versus 6%) in centers with expertise in pediatric pathology. This highlights the importance of the standardization of postmortem evaluations used to diagnose pediatric deaths. This might be undertaken by professionals with expertise in pediatrics and NAI. The importance of standardization is illustrated by the case report included in Case 1. This case demonstrated clearly that a postmortem physical exam was not sufficient to diagnose abusive head trauma, which was found only after the child underwent a postmortem computed tomography scan, which led to a legally mandated autopsy.

Another reason to standardize postmortem evaluations is that the risk of missing NAI in young children is higher compared to older children, mainly because of physiological differences between these age groups. While babies and toddlers are developing muscle strength, their bony structures remain more malleable [26]. Subtle signs of trauma can be masked and may be externally invisible. Furthermore, blunt abdominal trauma can lead to severe intra-abdominal injuries without any bruises on the abdominal wall [27, 28] and intrathoracic injuries frequently remain undetected in postmortem physical examinations [29]. Twelve of the 21 children in our study had no visible external injuries at admission; all of these were children who were younger than two years of age. Injuries were identified in nine of these children via additional investigations in the ED (including traumatic brain injury, retinal hemorrhage, and healing rib fractures). Injuries leading to death were revealed by postmortem radiologic studies and autopsy in the remaining three children although they exhibited no external injuries (fractures, traumatic brain injury, or signs of suffocation). While fatal NAI can and does occur in older children, more force is needed to produce the same type of fatal injury compared to that needed to injure younger children.

Another important finding in our study was the proportion of children suffering from neglect. The main cause of negligent deaths was drowning (78%). Examples of these cases include infants left alone in the bathtub or young children permitted to play near a pond or swimming pool with interrupted supervision. Our aim is not to accuse caregivers; however, we identified a large group (10%) of children whose deaths could have been prevented if sufficient supervision and appropriate preventive measures were taken. The aim of identifying situations associated with negligence will be to engage in conversations with the broader society, optimize education, and increase awareness of these dangers with the goal of prevention. We observed that many caregivers overestimated the capabilities of children and/or underestimated the danger involved in a given situation. As physicians, we must acknowledge these dangers and provide counseling to caregivers. As shown by our data, the danger of water, notably in water-rich countries such as the Netherlands, was largely underestimated. Many of the drownings might have been prevented by placing a fence around the pool or pond. This is mandatory in some European countries. We highly recommend reevaluation of the current guidelines by the Dutch legislature to raise national awareness of this topic. This would also focus on improving the educational programs available for caregivers and immigrants.

This nationwide study comprises a large cohort of cases of unnatural pediatric deaths due to NAI and AI. We were able to generate a multidisciplinary overview of this population and fatal NAI in the Netherlands in general. The Dutch national trauma registration data collection is of high quality as is postmortem information collected by forensic physicians. Because of this collaboration, the data collected represented an amalgamation of clinical information from 11 hospitals and information from forensic physicians combined with findings from legally mandated autopsies provided by NFI. By merging these sources of information, we identified significant indicators of fatal NAI. In addition, our expert panel consisted of a balanced group of physicians from different specialties (including child abuse, pediatric surgery, trauma surgery, pediatric forensic radiology, forensic medicine, and pediatrics). We believe that all cases were assessed carefully by the members of this panel.

One limitation of this study is that we only collected data from cases of children who died while in a hospital, i.e. selection bias. To address this issue, we compared our results to the national death registration maintained by Statistics Netherlands [5]. A rough estimate revealed that approximately half of the children who succumbed to trauma did so outside a Level I TC. We hypothesize that these children most likely died due to major trauma associated with excessive force, for example, severe accidents (high-speed motor vehicle crashes), prolonged drownings, or inflicted trauma of a very serious nature (such as a fall from a great height). Moreover, we had to classify some cases as indeterminate because we did not have data that would permit the expert panel to reach specific conclusions. Furthermore, we were unable to identify household characteristics that might be associated with NAI. We were able to provide a rough estimate of socioeconomic status based on the patients’ postal code and residential neighborhood.

Another common limitation in the child abuse field is the lack of a diagnostic “gold standard”. We attempted to use a diagnostic-type method using the information provided by CAN-teams, forensic physicians, courtrooms, and the consensus opinions of the expert panel. While we considered the conclusions of the CAN-team to be accurate, in most cases we did not have any insight into the specific information used by the CAN-team to generate their conclusions. This limitation may have led to an overestimation of the population subjected to NAT. Moreover, both CAN-teams and the expert panel considered injuries in their assessment. While this may have resulted in circular reasoning, in some cases, investigations were limited and injuries could have been missed. Nonetheless, consensus opinions of expert panels have been identified as a reliable means of assessing cases [30].

Finally, we assume that we may have underestimated the prevalence of fatal NAI in this study because we have reasons to doubt the effectiveness of the postmortem system in the Netherlands for detecting NAI. It is critical to recognize that no postmortem investigations are conducted in cases in which there are no suspicions of criminal behavior (Fig. 1). However, postmortem analyses from these cases could provide valuable information regarding what may be undetected criminal acts. According to the European Autopsy rules of the Council of Europe Committee of Ministers (CECM) and the European Council of Legal Medicine (ECLM), while each member state needs to have an effective means to investigate deaths, each is provided with some independence regarding the design of this system [7]. Of course, every design has benefits and consequences. In the system currently in use in the Netherlands, the treating physician, the DA, and the forensic physician all play crucial roles in the determination of the cause and manner of death. Cases of NAI are likely missed because of a lack of awareness. Thus, the consequences of this system include the fact that we are at risk of missing non-accidental fatalities among our most vulnerable residents and thereby create insufficient awareness of this critical health problem. A recent NFI report documented that, based on decreasing numbers of autopsies, an estimated 20–25 murder cases were missed in the Netherlands in the year 2015 alone [31]. As noted in our study, the limited use of postmortem investigations may very likely have resulted in an underestimation of non-accidental cases of pediatric death.

Current law in the Netherlands requires a review of every pediatric death by a forensic physician. However, in practice, this is only done in ~ 70% of relevant cases [32]. This is another potential source of missed NAI cases, as it is clear that some cases were not reported to the forensic physician. Most cases underwent an external postmortem physical examination but no postmortem investigations (NB only 21% underwent postmortem investigations). As previously discussed, we advocate the more extensive use of postmortem investigations in cases of pediatric death. This exercise will be pivotal for diagnostic accuracy and for determining the cause and manner of death.

In this nationwide Level I TC study, we identified NAI in 20% of children who experienced an unnatural death during a five-year period (January 2014 – December 2018). NAI was identified as the cause of 44% of the deaths in preschool-aged children (< 5 years old). Postmortem investigations were performed in only one of five children who died at the hospital. Of note, no data are available for the 50% of trauma-associated childhood deaths that took place outside a Level I TC. This may have resulted in an underestimate of the frequency of fatal NAI. Furthermore, our studies suggest strongly that a postmortem physical exam alone will not provide enough evidence to rule out the possibility of inflicted trauma in young children who have died as a result of unwitnessed trauma or under circumstances that are not fully clear. In these cases, we recommend more extensive postmortem investigations to rule out any possibility of inflicted death. Among these, cases of serial drownings should raise concerns regarding dangers in the environment and the potential lack of appropriate supervision. Educational programs focused on pediatric health and safety might be offered to caregivers by midwives, pediatricians, or general physicians.