REVIEW URRENT C OPINION
Update on abusive head trauma Ashkon Shaahinfar a,b, Kevin D. Whitelaw a,b, and Karim M. Mansour a,b
Purposes of review This article provides an update on abusive head trauma (AHT), focusing on new developments most salient to the emergency medicine clinician, including epidemiology, clinical recognition, diagnostic work-up, management of neurologic injury, and public health implications. Recent findings The recent literature has focused on honing the clinician’s ability to recognize AHT and its immediate sequelae, to more accurately distinguish between abusive and accidental head injuries by patterns of neuroimaging and retinal hemorrhages, and to appreciate the long-term impacts. Specifically, both a clinical prediction rule and biomarker show promise, and new research advocates for the early identification of subclinical seizures as well as cervical spine injuries. Summary The emergency medicine provider must be able to recognize and manage children who may have AHT and to appreciate when the diagnostic findings warrant consultation with a child protection team. These authors summarize the recent and notable advances in our understanding of AHT. Keywords abusive head trauma, pediatric traumatic brain injury, retinal hemorrhages, subdural hematoma
INTRODUCTION
EPIDEMIOLOGY
Abusive head trauma (AHT) is responsible for a significant majority of serious traumatic brain injuries in children younger than age 2 with high rates of morbidity and mortality [1–3]. Often these infants and children present to the emergency department (ED), where they may demonstrate a wide range of symptoms, from nonspecific to severe, making accurate and prompt recognition a substantial challenge for providers [4]. Since Caffey’s classic description of subdural hematomas (SDHs), retinal hemorrhages, and metaphyseal fractures due to ‘whiplash shaken infant syndrome’ [5], decades of research and debate have ensued, leading to a policy statement by the American Academy of Pediatrics advocating for the use of the term AHT to describe inflicted injury to the head of an infant or child, whether by violent shaking, blunt impact, or both [6]. The recent literature has continued to reinforce our understanding of the epidemiology of AHT. Notable developments have been made that may aid clinicians in its early identification, accurate diagnose, and acute management. Finally, efforts continue in assessing the long-term impacts of AHT and developing effective prevention programs.
The Centers for Disease Control and a panel of experts recently developed standardized guidelines for the use of International Classification of Disease (ICD-9 and ICD-10) codes for researchers to study the epidemiology of AHT, addressing prior inconsistencies in its definition and measurement [7]. Since their publication in 2012, these guidelines have been utilized in various studies, including a recent nationwide sample drawn from the Kids’ Inpatient Database by Shanahan et al. [8], which found an annual incidence of 33.4–38.8 cases per 100 000 children less than 1 year of age. Using both hospital discharge and ED datasets from South Carolina for 2000–2010, Selassie et al. [9 ] applied a similar set of ICD-9 codes and found
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a Department of Emergency Medicine, UCSF Benioff Children’s Hospital Oakland, Oakland and bDepartment of Emergency Medicine, UCSF, San Francisco, California, USA
Correspondence to Ashkon Shaahinfar, MD, MPH, Department of Emergency Medicine, UCSF Benioff Children’s Hospital Oakland, 747 52nd St, Oakland, CA 94609, USA. Tel: +1 510 428 3259; fax: +1 510 450 5836; e-mail: [email protected] Curr Opin Pediatr 2015, 27:308–314 DOI:10.1097/MOP.0000000000000207 Volume 27 Number 3 June 2015
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Update on abusive head trauma Shaahinfar et al.
KEY POINTS With recent standardization of the definition and measurement of AHT, researchers continue to build our understanding of its epidemiology, outcomes, costs, and prevention, including the high rate of missed opportunities in the ED. A validated clinical prediction rule, as well as a serum biomarker, have the potential to sharpen the ability of clinicians to recognize occult cases of AHT and initiate further diagnostic work-up. The evidence base continues to grow toward more accurate differentiation between AHT and other diagnoses through neuroimaging and retinal findings, including the use of MRI. AHT should be considered in children and infants with otherwise unexplained subclinical seizures, status epilepticus, and cervical spine injuries.
that the incidence of AHT ranged from 28.0 per 100 000 in infants to 4.1 per 100 000 in 5-year-old children. Importantly, the authors highlight that 42% of AHT was captured from the ED data, a subpopulation that tended to be older and to have less severe injuries, emphasizing both the challenge and importance of ED providers maintaining a high suspicion for AHT. Ortega et al. [10] compared a sample of 124 patients treated for accidental or abusive fatal injuries in two, urban pediatric EDs between 1998 and 2010. Coinciding with existing literature on nonfatal AHT, children with abusive fatal injuries were younger (11 months versus 4 years 9 months) and more likely to be seen in a clinic or ED in the prior 2 months (51 versus 5.8%), highlighting the possibility of delayed diagnoses and missed opportunities for prevention.
of 291 acutely head-injured children less than 3-years old admitted to 14 pediatric ICUs (PICUs) in the Pediatric Brain Injury Research Network. The rule included four variables: acute respiratory compromise any time prior to admission; bruising of the ears, neck, or torso; bilateral or interhemispheric subdural hemorrhages or fluid collections; and any skull fractures aside from isolated, unilateral, nondiastatic, linear, and parietal fractures. In this validation population, which excluded children injured in motor vehicle accidents and those with preexisting brain conditions, presenting with one or more of the four variables carried a sensitivity of 96% and a specificity of 43% for AHT in comparison to a priori definitional criteria for AHT and identified 98% of the 144 children ultimately diagnosed with AHT. According to the authors, this screening rule is meant to capture nearly all children who should undergo further diagnostic evaluation for potential abuse. Historical clues, such as denial of accidental or inflicted head trauma, inconsistency of the history with the child’s gross motor skills, or variation in historical details over time, prompted evaluation of the three children with AHT missed by the rule.
Abusive versus accidental head trauma by head injury pattern
As exemplified in a recent case report by Tilak and Pollock [11] from the pediatric emergency medicine literature, patients with AHT may present with seemingly unrelated and nonspecific complaints, making its recognition and diagnosis particularly challenging. The recent literature has made important strides toward strengthening the ability of clinicians to identify AHT.
The body of AHT literature supports an understanding that subdural hemorrhage that is either unexplained or not related to comorbidity [such as macrocrania [14] and increased intracranial pressure (ICP) [15]] warrants raised suspicion for nonaccidental trauma. In an effort to build upon and further clarify this literature, Roach et al. [16 ] retrospectively reviewed the largest case series of AHT to date, 580 young children over the course of 16 years. Patients with AHT were significantly less likely than those with accidental injury to have skull fractures (22 versus 52%) and epidural hematomas (3 versus 11%) and significantly more likely to have diffuse axonal injury (14 versus 8%) and SDH (76 versus 23%). Of course, given that the child protection team likely incorporated head injury pattern into their diagnosis of AHT, it is not possible to avoid circularity of reasoning in these findings. From the emergency medicine perspective, head injury pattern can modify suspicion for AHT and guide the decision about whether or not to seek further expert consultation.
A validated clinical prediction rule among head-injured children
A prospective biomarker for mild abusive head trauma
CLINICAL RECOGNITION
Having previously derived a clinical prediction rule to screen for AHT [12], Hymel et al. [13 ] prospectively validated the rule in a new population &&
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Clinical prediction rules and radiologic findings that distinguish abusive from accidental head trauma rely in large part on the recognition of acute
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head injury. However, given that AHT often presents with nonspecific symptoms, without external sign of injury, and without a disclosed history of head trauma, researchers hope that certain serum biomarkers might help identify more subtle cases of AHT just as transaminases are used to screen for occult abdominal trauma [17]. Gao et al. [18 ] compared serum proteomic profiles of patients diagnosed with mild AHT [Glasgow Coma Scale (GCS) 13–15] who presented for the evaluation of head trauma or a neurologic symptom (e.g., vomiting, fussiness, or seizures) with those of matched controls presenting with similar symptoms but without a history of head trauma or diagnosis of brain injury. Serum amyloid A, an acute phase reactant previously identified as a potential marker of injury in hypoxic-ischemic encephalopathy and traumatic brain injury (TBI), had significantly higher mean expression among AHT cases versus controls, with impressive discriminating ability and an area under the receiver operator curve of 0.96. &&
DIAGNOSTIC WORK-UP According to a recent, comprehensive review by Ryan et al. [19 ] with the American College of Radiology, noncontrast head computed tomography (CT) is indeed the initial study of choice for suspected AHT. Furthermore, in the absence of neuroimaging findings, recent evidence by Greiner et al. [20] supports deferral of dedicated retinal exam. The radiology and ophthalmology literature relating to the diagnosis of AHT continues to grow. &&
Patterns of intracranial injury in abusive head trauma The neuroradiologic finding of hemispheric hypodensity in association with SDH has been previously described in AHT and is known to be associated with poor outcomes [21,22]. Foster et al. [23 ] have attempted to identify clinical risk factors for hemispheric hypodensity in AHT patients with SDH. In their study of 24 children with AHT, 13 developed hemispheric hypodensity. Daily ICP maximums and intensity of ICP monitoring were significantly higher in patients with hemispheric hypodensity than those without hemispheric hypodensity. Hypoxia, hypotension, and cardiopulmonary arrest, need for blood transfusions and daily blood glucose levels, tended to be higher in the hemispheric hypodensity patients, though not significantly so. The underlying pathophysiology of hemispheric hypodensity remains unknown. Sieswerda-Hoogendoorn et al. [24 ] compared 54 AHT victims with impact head trauma, indicated by scalp soft-tissue injury or skull fracture, with 45 AHT victims without clinical &
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evidence of impact. Children with skull fractures had fewer hypoxic-ischemic injuries than those without fractures (33 versus 57%), but there were no other significant differences in neuroradiological or musculoskeletal findings between impact and nonimpact cases, suggesting that the determination of injury mechanism is not straightforward.
Forensic use of neuroimaging Thomas et al. [25] studied 149 patients, less than 2 years of age, with accidental head injury. Many had skull fractures (36%), about one third of whom had thin, underlying SDH. Only two patients had isolated SDH without skull fracture. All patients who had radiologically identified parenchymal injuries, including hypoxic-ischemic, or severe neurologic sequelae had corresponding high-force mechanisms of injury, supporting the dismissal of minor mechanisms of trauma as potential explanations of severe intracranial injuries. CT and MRI have been used forensically in an attempt to determine the age of SDH in possible AHT patients. Sieswerda-Hoogendoorn et al. [26] performed a literature review of 22 studies describing SDHs on CT, and four on MRI, concluding that, at present, evidence does not support using these imaging modalities to determine the age of SDH.
Utility of MRI In addition to the identification of cervical spine injuries and retinal hemorrhages, discussed below, the use of MRI in the diagnosis and prognostication of AHT has an expanding literature base. In their cohort of 74 children less than 36 months with head trauma, Kadom et al. [27 ] found a significant association between bilateral hypoxic-ischemic injury pattern and AHT, hypothesized to be because of injury at the craniocervical junction resulting in apnea and hypoxia [28]. Diffusion MRI is a technique of mapping of the diffusion of molecules in tissues, with low diffusion measurements in the brain signifying tissue damage. Imagawa et al. [29] used diffusion tensor imaging in 17 infants with AHT and 34 control infants of similar postconceptual age who underwent MRI for other indications. Reduced ‘axial diffusivity’ was found widespread in the white matter of AHT patients compared with controls, and was worse in the patients with severe outcomes than mild/moderate outcomes, findings with potential for diagnostic and prognostic applications. &&
Differential diagnosis for retinal hemorrhages It is well known that retinal hemorrhages are encountered in up to 50–100% of children who Volume 27 Number 3 June 2015
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Update on abusive head trauma Shaahinfar et al.
have sustained an abusive head injury [30]; however, retinal hemorrhages are not exclusive to AHT and have previously been reported in other conditions (e.g. [14,15]) with varying prevalence. In a study examining a prospective cohort of over 2000 vaginal births, Laghmari et al. [31 ] reported nearly one third of healthy newborns exhibited retinal hemorrhages. The hemorrhages tended to be few in number and localized to the optic discs and posterior pole of the retina. Furthermore, the majority of the hemorrhages had resolved within 1 week of birth and all had resolved within 4 weeks. In the nonabused critically ill child, a 15% prevalence of retinal hemorrhages has been reported, with more severe, widespread findings rarely occurring [32]. Specifically examining the critically ill intubated child, Longmuir et al. [33] reported an even lower prevalence of retinal hemorrhages; without a history of trauma, diffuse multilayered hemorrhages were not found. Understanding how retinal hemorrhages present in various clinical conditions may influence the need for further AHT investigation. &
Mechanism for retinal injury and standardizing retinal findings As demonstrated in recent experimental models by Yamazaki et al. [34], the primary proposed mechanism for the widespread, multilayered retinal hemorrhages in children who undergo shaking with violent, rotational movements of the eyes, is that the vitreous humor exerts extreme traction on the retina, in contrast with unidirectional/blunt head trauma, which generally results in few or no retinal hemorrhages [35]. Levin et al. [36 ] developed a web-based tool to document the various characteristics of retinal hemorrhages, in an effort to establish a universally accepted standard for recording retinal findings. The investigators reported high interobserver and intraobserver reliability among pediatric ophthalmologists. Zuccoli et al. [37] compared susceptibility weighted MRI to the dilated fundoscopic exam, the gold standard, at identifying retinal hemorrhages. The authors reported an MRI sensitivity of 83%, supporting its potential as a diagnostic tool and its utility when a dilated fundoscopic exam is not possible. In a cohort of children with suspected AHT, Longmuir et al. [38 ] found that a quantitative measurement of the area of retinal hemorrhages was significantly higher in children with axial skeletal fractures, with signs of severe brain trauma on neuroimaging, and with definite versus possible abuse, findings which have potential medicolegal implications.
MANAGEMENT OF NEUROLOGIC INJURY Recent publications in the neurology, orthopedics, and neurosurgery literature have emphasized the importance of early identification and treatment of the immediate neurologic sequelae that can be associated with AHT in infants and young children.
Subclinical seizures and status epilepticus Although clinical seizures are a known complication of AHT, less is known about the prevalence of subclinical seizures in these children. Hasbani et al. [39] conducted a retrospective review of 32 children 2 years of age and younger admitted to the PICU with AHT. Of the 21 patients who underwent electroencephalographic (EEG) monitoring, 12 had electrographic seizures, eight had only nonconvulsive seizures on EEG, and eight experienced electrographic status epilepticus. Though limited by a small sample size, no significant association was detected between the presence of electrographic seizures and either clinical seizures at presentation or abnormalities on neuroimaging. Drawing from a larger, prospective cohort of 87 patients admitted to the PICU for acute, mild to severe TBI who underwent continuous EEG monitoring by protocol, Arndt et al. [40 ] found that younger age, AHT, and intraaxial bleed were risk factors for both status epilepticus and subclinical status epilepticus. Further urging a high index of suspicion for AHT in infants with seizures or status epilepticus, Fernandez-Menendez et al. [41] presented case reports of two young infants who were ultimately diagnosed with AHT after developing status epilepticus in the context of intercurrent febrile respiratory infections. &&
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Associated spinal injuries Aside from vertebral plain films in the skeletal survey, screening for more subtle spinal injuries is not a routine component of the AHT work-up, and two recent retrospective studies would advocate otherwise [27 ,42 ]. Knox et al. [42 ] reviewed all pediatric cases of spinal trauma diagnosed over 9 years at a level 1 trauma center. They found that 11 of 342 (3.2%) cases were caused by nonaccidental trauma and that this was tied with motor vehicle collisions as the most common mechanism among children under age 2. Eight of these children had associated head trauma. Taking a complementary approach, Kadom et al. [27 ] reviewed 74 cases of head trauma in children less than 3 years of age in which the child abuse team became involved and both brain and cervical spine MRI were obtained. Thirty-six percent of patients were found to have cervical spine injuries, which were predominantly
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ligamentous but also included three patients with more severe injuries. Cervical spine injury, although seen in most patients with bilateral hypoxic-ischemic brain injury from AHT, did not distinguish between abusive and accidental head trauma. Given the high incidence of cervical spine injury in children with suspected AHT, the authors argue that its presence may be useful in differentiating between traumatic and atraumatic SDH.
from a nationwide health insurance claim database, Peterson et al. [45 ] contributed significantly to our understanding of costs attributed to AHT. They found that AHT was associated with significantly greater medical service use and higher inpatient, outpatient, drug, and total cost over multiple years. They estimated that the excess cost attributable to AHT over 4 years following diagnosis was $47 952 per patient.
Neurosurgical intervention for traumatic subdural hematoma
Primary prevention of abusive head trauma
There is no standardized protocol for the neurosurgical treatment of traumatic SDH secondary to AHT in children younger than 2 years of age, though potential indications include signs of intracranial hypertension, large hematoma size (e.g. >10 mm), and low GCS (e.g. GCS 12). Melo et al. [43] described their own experiences treating 184 children younger than 2 years admitted to the neurosurgical PICU with traumatic SDH on CT concerning for AHT. Sixty percent underwent emergency neurosurgical intervention. Craniotomy and decompressive craniectomy were only completed in two cases, respectively, all with massive acute SDH and severe intracranial hypertension. Subdural puncture and external subdural drainage proved to provide only transient stabilization in many patients, who commonly required definitive treatment with subdural-peritoneal or subduralsubgaleal shunt.
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Although most of the evidence regarding child abuse prevention centers around secondary prevention for at-risk children through home visiting programs, most publications this year related to AHT have reported on more broadly directed, primary prevention efforts conducted in the clinical setting. Simonnet et al. [46] found that a short talk and pamphlet on infant crying and AHT during 190 routine newborn examinations was feasible, acceptable, and significantly improved parental knowledge. Allen [47 ] conducted a systematic review of 10 similar newborn interventions and described two studies, published in 2005 [48] and 2011 [49], respectively, which were able to demonstrate significant decreases in AHT rate post-intervention. These findings suggest an important opportunity for educational interventions directed toward parents of newborns seen in the ED. &
CONCLUSION PUBLIC HEALTH IMPLICATIONS As with other forms of abuse and neglect, there has been ongoing research to measure the longterm impacts of AHT, which further underscores the need to develop and evaluate effective prevention efforts.
Outcomes and costs of abusive head trauma Risen et al. [44] compared functional outcomes in 28 AHT patients with age-matched and sex-matched controls with non-AHT admitted to the same inpatient rehabilitation unit. Though the two cohorts had similar brain injuries, the AHT group had more associated injuries with the potential for neurologic sequelae, including status epilepticus. Although similar proportions of children greater than 12 months of age in both groups attained independent ambulation and expressive language by time of discharge, significantly fewer children with AHT ultimately achieved these outcomes. Drawing 1209 patients with AHT and 5895 matched controls 312
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AHT is a complex diagnosis, with social, legal, and medical implications, and a 70 year, often contentious history in the medical literature [50]. With this expanding body of literature and the support of future studies, there is hope that clinicians, including those in the ED, may be more and more equipped to accurately and effectively recognize, diagnose, and manage this often occult injury. In light of the sobering costs to these children and the healthcare system, additional resources should be dedicated toward developing and evaluating effective prevention efforts. Acknowledgements None. Financial support and sponsorship None. Conflicts of interest There are no conflicts of interest. Volume 27 Number 3 June 2015
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Update on abusive head trauma Shaahinfar et al.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Duhaime AC, Alario AJ, Lewander WJ, et al. Head injury in very young children: mechanisms, injury types, and ophthalmologic findings in 100 hospitalized patients younger than 2 years of age. Pediatrics 1992; 90:179–185. 2. Billmire ME, Myers PA. Serious head injury in infants: accident or abuse? Pediatrics 1985; 75:340–342. 3. Bruce DA, Zimmerman RA. Shaken impact syndrome. Pediatr Ann 1989; 18:482–484; 486–489, 492–494. 4. Jenny C, Hymel KP, Ritzen A, et al. Analysis of missed cases of abusive head trauma. JAMA 1999; 281:621–626. 5. Caffey J. The whiplash shaken infant syndrome: manual shaking by the extremities with whiplash-induced intracranial and intraocular bleedings, linked with residual permanent brain damage and mental retardation. Pediatrics 1974; 54:396–403. 6. Christian CW, Block R; Committee on Child Abuse and Neglect, American Academy of Pediatrics. Abusive head trauma in infants and children. Pediatrics 2009; 123:1409–1411. 7. Parks SE, Annest JL, Hill HA, Karch DL. Pediatric abusive head trauma: recommended definitions for public health surveillance and research. Atlanta, GA: Centers for Disease Control and Prevention; 2012. pp. 5–16. 8. Shanahan ME, Zolotor AJ, Parrish JW, et al. National, regional, and state abusive head trauma: application of the CDC algorithm. Pediatrics 2013; 132:e1546–e1553. 9. Selassie AW, Borg K, Busch C, Russell WS. Abusive head trauma in young & children: a population-based study. J Trauma Nurs 2014; 21:72–82. This is the first population-based study to use both hospital and ED databases to estimate AHT incidence and determine relevant risk factors, highlighting the need to include ED patients to capture less severe cases of AHT. 10. Ortega HW, Vander Velden H, Kreykes NS, Reid S. Childhood death attributable to trauma: is there a difference between accidental and abusive fatal injuries? J Emerg Med 2013; 45:332–337. 11. Tilak GS, Pollock AN. Missed opportunities in fatal child abuse. Pediatr Emerg Care 2013; 29:685–687. 12. Hymel KP, Willson DF, Boos SC, et al. Derivation of a clinical prediction rule for pediatric abusive head trauma. Pediatr Crit Care Med 2013; 14:210–220. 13. Hymel KP, Armijo-Garcia V, Foster R, et al. Validation of a clinical prediction && rule for pediatric abusive head trauma. Pediatrics 2014; 134:e1537–e1544. Although not obviating the need for clinical reasoning, the authors have validated a highly sensitive clinical prediction rule using four variables readily available at time of admission to the PICU to reliably detect and prompt work-up for potential AHT. Given its high sensitivity and relatively low specificity, the rule is meant to be implemented as a screening tool. 14. Greiner MV, Richards TJ, Care MM, Leach JL. Prevalence of subdural collections in children with macrocrania. AJNR Am J Neuroradiol 2013; 34:2373–2378. 15. Binenbaum G, Rogers DL, Forbes BJ, et al. Patterns of retinal hemorrhage associated with increased intracranial pressure in children. Pediatrics 2013; 132:e430–e434. 16. Roach JP, Acker SN, Bensard DD, et al. Head injury pattern in children can & help differentiate accidental from nonaccidental trauma. Pediatr Surg Int 2014; 30:1103–1106. The largest reported series to date of children with AHT, this retrospective comparative cohort study further supports the present understanding that the presence of SDH or diffuse axonal injury should raise suspicion for AHT, including in children under age 2. 17. Lindberg DM, Shapiro RA, Blood EA, et al., ExSTRA investigators. Utility of hepatic transaminases in children with concern for abuse. Pediatrics 2013; 131:268–275. 18. Gao W, Lu C, Kochanek PM, Berger RP. Serum amyloid A is increased in && children with abusive head trauma: a gel-based proteomic analysis. Pediatr Res 2014; 76:280–286. Addressing the subset of patients who have no history of trauma and would otherwise be easily missed, this is the first study to compare the serum proteomic profile of children with AHT and matched controls without brain injury. The findings suggest that a child with soft neurologic signs such as vomiting, fussiness, or seizures might require head CT to evaluate for head trauma if their serum amyloid A expression is high. 19. Ryan ME, Palasis S, Saigal G, et al. ACR appropriateness criteria head && trauma–child. J Am Coll Radiol 2014; 11:939–947. Updated, evidence-based guidelines by the American College of Radiology to assist physicians in making imaging decisions across various modalities for pediatric head trauma, including suspected nonaccidental head trauma. 20. Greiner MV, Berger RP, Thackeray JD, Lindberg DM; Examining Siblings to Recognize Abuse (ExSTRA) Investigators. Dedicated retinal examination in children evaluated for physical abuse without radiographically identified traumatic brain injury. J Pediatr 2013; 163:527–531.
21. Duhaime AC, Bilaniuk L, Zimmerman R. The ‘‘big black brain’’: radiographic changes after severe inflicted head injury in infancy. J Neurotrauma 1993; 10 (Suppl 1):S59. 22. Duhaime AC, Durham S. Traumatic brain injury in infants: the phenomenon of subdural hemorrhage with hemispheric hypodensity (‘‘Big Black Brain’’). Prog Brain Res 2007; 161:293–302. 23. Foster KA, Recker MJ, Lee PS, et al. Factors associated with hemispheric & hypodensity after subdural hematoma following abusive head trauma in children. J Neurotrauma 2014; 31:1625–1631. This study takes important steps in identifying clinical risk factors for hemispheric hypodensity, a poorly understood and highly fatal complication after SDH in the AHT population. 24. Sieswerda-Hoogendoorn T, Robben SG, Karst WA, et al. Abusive head & trauma: differentiation between impact and nonimpact cases based on neuroimaging findings and skeletal surveys. Eur J Radiol 2014; 83:584– 588. This retrospective study questions whether neuroimaging and skeletal survey findings contribute much beyond external signs of head trauma (including skull fracture) to the determination of whether a case of AHT occurred by impact or nonimpact mechanism. 25. Thomas AG, Hegde SV, Dineen RA, Jaspan T. Patterns of accidental craniocerebral injury occurring in early childhood. Arch Dis Child 2013; 98:787–792. 26. Sieswerda-Hoogendoorn T, Postema FA, Verbaan D, et al. Age determination of subdural hematomas with CT and MRI: a systematic review. Eur J Radiol 2014; 83:1257–1268. 27. Kadom N, Khademian Z, Vezina G, et al. Usefulness of MRI detection of && cervical spine and brain injuries in the evaluation of abusive head trauma. Pediatr Radiol 2014; 44:839–848. The largest cohort of children evaluated for AHT for which the rate of cervical spine soft-tissue injuries was determined, this article adds significantly to the literature regarding the use of MRI in screening for AHT. The findings support the idea that bilateral hypoxic-ischemic injury as well as cervical injury on MRI may help distinguish between abusive and accidental head trauma, depending on the clinical scenario. 28. Geddes JF, Vowles GH, Hackshaw AK, et al. Neuropathology of inflicted head injury in children. II. Microscopic brain injury in infants. Brain 2001; 124:1299–1306. 29. Imagawa KK, Hamilton A, Ceschin R, et al. Characterization of microstructural injury: a novel approach in infant abusive head trauma-initial experience. J Neurotrauma 2014; 31:1632–1638. 30. Binenbaum G, Forbes BJ. The eye in child abuse: key points on retinal hemorrhages and abusive head trauma. Pediatr Radiol 2014; 44 (Suppl 4): 571–577. 31. Laghmari M, Skiker H, Handor H, et al. Birth-related retinal hemorrhages in the & newborn: incidence and relationship with maternal, obstetric and neonatal factors. Prospective study of 2031 cases. J Fr Ophtalmol 2014; 37:313– 319. An exceptionally large, prospective cohort of over 2000 newborns examined for retinal hemorrhages, further supporting typical characteristics of, and risk factors for, birth-related retinal hemorrhages previously described in the literature and highlighting, with greater confidence, that these hemorrhages only very rarely last beyond 1 month of age. 32. Agrawal S, Peters MJ, Adams GG, Pierce CM. Prevalence of retinal hemorrhages in critically ill children. Pediatrics 2012; 129:e1388– e1396. 33. Longmuir SQ, McConnell L, Oral R, et al. Retinal hemorrhages in intubated pediatric intensive care patients. J AAPOS 2014; 18:129–133. 34. Yamazaki J, Yoshida M, Mizunuma H. Experimental analyses of the retinal and subretinal haemorrhages accompanied by shaken baby syndrome/ abusive head trauma using a dummy doll. Injury 2014; 45:1196– 1206. 35. Morad Y, Wygnansky-Jaffe T, Levin AV. Retinal haemorrhage in abusive head trauma. Clin Experiment Ophthalmol 2010; 38:514–520. 36. Levin AV, Cordovez JA, Leiby BE, et al. Retinal hemorrhage in abusive head & trauma: finding a common language. Trans Am Ophthalmol Soc 2014; 112:1–10. This article makes significant progress toward standardizing the description of retinal finding in order to develop a common language for related clinical, educational, and research purposes. 37. Zuccoli G, Panigrahy A, Haldipur A, et al. Susceptibility weighted imaging depicts retinal hemorrhages in abusive head trauma. Neuroradiology 2013; 55:889–893. 38. Longmuir SQ, Oral R, Walz AE, et al. Quantitative measurement of retinal & hemorrhages in suspected victims of child abuse. J AAPOS 2014; 18:529– 533. Adding an additional level of objectivity to the characterization of retinal hemorrhages, this study is the first to demonstrate that semiautomated quantification of retinal hemorrhages correlates with risk factors for, the definitive diagnosis of, and the neurologic injury from AHT. 39. Hasbani DM, Topjian AA, Friess SH, et al. Nonconvulsive electrographic seizures are common in children with abusive head trauma. Pediatr Crit Care Med 2013; 14:709–715.
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Emergency and critical care medicine 40. Arndt DH, Lerner JT, Matsumoto JH, et al. Subclinical early posttraumatic seizures detected by continuous EEG monitoring in a consecutive pediatric cohort. Epilepsia 2013; 54:1780–1788. The first multicenter, prospective study of the incidence and risk factors for early posttraumatic seizures as measured by EEG, with important implications for the management of AHT patients. AHT patients appear to be at particularly high risk for subclinical seizures and status epilepticus and should be appropriately screened. 41. Fernandez-Menendez A, Buenache-Espartosa R, Coca-Perez A, et al. Refractory status epilepticus presenting as shaken baby syndrome. Rev Neurol 2014; 58:548–552. 42. Knox J, Schneider J, Wimberly RL, Riccio AI. Characteristics of spinal injuries & secondary to nonaccidental trauma. J Pediatr Orthop 2014; 34:376–381. Though spinal injuries appear to be uncommon in nonaccidental trauma, this retrospective series highlights important epidemiologic and clinical features to help avoid missed diagnoses. 43. Melo JR, Di Rocco F, Bourgeois M, et al. Surgical options for treatment of traumatic subdural hematomas in children younger than 2 years of age. J Neurosurg Pediatr 2014; 13:456–461. 44. Risen SR, Suskauer SJ, Dematt EJ, et al. Functional outcomes in children with abusive head trauma receiving inpatient rehabilitation compared with children with nonabusive head trauma. J Pediatr 2014; 164:613–619.e1-2.
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45. Peterson C, Xu L, Florence C, et al. The medical cost of abusive head trauma in the United States. Pediatrics 2014; 134:91–99. Using a novel methodology to incorporate both inpatient and outpatient aspects of healthcare costs that victims of AHT endure, the findings of this article may prove powerful in advocating for cost-effective prevention efforts. 46. Simonnet H, Laurent-Vannier A, Yuan W, et al. Parents’ behavior in response to infant crying: abusive head trauma education. Child Abuse Negl 2014; 38:1914–1922. 47. Allen KA. The neonatal nurse’s role in preventing abusive head trauma. Adv & Neonatal Care 2014; 14:336–342. In this systematic review of primary AHT prevention efforts involving neonatal nurses, attention is drawn to two interventions which show scientific promise in decreasing AHT and the potential to be adapted to diverse settings. 48. Dias MS, Smith K, DeGuehery K, et al. Preventing abusive head trauma among infants and young children: a hospital-based, parent education program. Pediatrics 2005; 115:e470–e477. 49. Altman RL, Canter J, Patrick PA, et al. Parent education by maternity nurses and prevention of abusive head trauma. Pediatrics 2011; 128:e1164– e1172. 50. Ingraham FD, Matson DD. Subdural hematoma in infancy. J Pediatr 1944; 24:1–37. &
Volume 27 Number 3 June 2015
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Update on abusive head trauma Ashkon Shaahinfar a,b, Kevin D. Whitelaw a,b, and Karim M. Mansour a,b
Purposes of review This article provides an update on abusive head trauma (AHT), focusing on new developments most salient to the emergency medicine clinician, including epidemiology, clinical recognition, diagnostic work-up, management of neurologic injury, and public health implications. Recent findings The recent literature has focused on honing the clinician’s ability to recognize AHT and its immediate sequelae, to more accurately distinguish between abusive and accidental head injuries by patterns of neuroimaging and retinal hemorrhages, and to appreciate the long-term impacts. Specifically, both a clinical prediction rule and biomarker show promise, and new research advocates for the early identification of subclinical seizures as well as cervical spine injuries. Summary The emergency medicine provider must be able to recognize and manage children who may have AHT and to appreciate when the diagnostic findings warrant consultation with a child protection team. These authors summarize the recent and notable advances in our understanding of AHT. Keywords abusive head trauma, pediatric traumatic brain injury, retinal hemorrhages, subdural hematoma
INTRODUCTION
EPIDEMIOLOGY
Abusive head trauma (AHT) is responsible for a significant majority of serious traumatic brain injuries in children younger than age 2 with high rates of morbidity and mortality [1–3]. Often these infants and children present to the emergency department (ED), where they may demonstrate a wide range of symptoms, from nonspecific to severe, making accurate and prompt recognition a substantial challenge for providers [4]. Since Caffey’s classic description of subdural hematomas (SDHs), retinal hemorrhages, and metaphyseal fractures due to ‘whiplash shaken infant syndrome’ [5], decades of research and debate have ensued, leading to a policy statement by the American Academy of Pediatrics advocating for the use of the term AHT to describe inflicted injury to the head of an infant or child, whether by violent shaking, blunt impact, or both [6]. The recent literature has continued to reinforce our understanding of the epidemiology of AHT. Notable developments have been made that may aid clinicians in its early identification, accurate diagnose, and acute management. Finally, efforts continue in assessing the long-term impacts of AHT and developing effective prevention programs.
The Centers for Disease Control and a panel of experts recently developed standardized guidelines for the use of International Classification of Disease (ICD-9 and ICD-10) codes for researchers to study the epidemiology of AHT, addressing prior inconsistencies in its definition and measurement [7]. Since their publication in 2012, these guidelines have been utilized in various studies, including a recent nationwide sample drawn from the Kids’ Inpatient Database by Shanahan et al. [8], which found an annual incidence of 33.4–38.8 cases per 100 000 children less than 1 year of age. Using both hospital discharge and ED datasets from South Carolina for 2000–2010, Selassie et al. [9 ] applied a similar set of ICD-9 codes and found
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a Department of Emergency Medicine, UCSF Benioff Children’s Hospital Oakland, Oakland and bDepartment of Emergency Medicine, UCSF, San Francisco, California, USA
Correspondence to Ashkon Shaahinfar, MD, MPH, Department of Emergency Medicine, UCSF Benioff Children’s Hospital Oakland, 747 52nd St, Oakland, CA 94609, USA. Tel: +1 510 428 3259; fax: +1 510 450 5836; e-mail: [email protected] Curr Opin Pediatr 2015, 27:308–314 DOI:10.1097/MOP.0000000000000207 Volume 27 Number 3 June 2015
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Update on abusive head trauma Shaahinfar et al.
KEY POINTS With recent standardization of the definition and measurement of AHT, researchers continue to build our understanding of its epidemiology, outcomes, costs, and prevention, including the high rate of missed opportunities in the ED. A validated clinical prediction rule, as well as a serum biomarker, have the potential to sharpen the ability of clinicians to recognize occult cases of AHT and initiate further diagnostic work-up. The evidence base continues to grow toward more accurate differentiation between AHT and other diagnoses through neuroimaging and retinal findings, including the use of MRI. AHT should be considered in children and infants with otherwise unexplained subclinical seizures, status epilepticus, and cervical spine injuries.
that the incidence of AHT ranged from 28.0 per 100 000 in infants to 4.1 per 100 000 in 5-year-old children. Importantly, the authors highlight that 42% of AHT was captured from the ED data, a subpopulation that tended to be older and to have less severe injuries, emphasizing both the challenge and importance of ED providers maintaining a high suspicion for AHT. Ortega et al. [10] compared a sample of 124 patients treated for accidental or abusive fatal injuries in two, urban pediatric EDs between 1998 and 2010. Coinciding with existing literature on nonfatal AHT, children with abusive fatal injuries were younger (11 months versus 4 years 9 months) and more likely to be seen in a clinic or ED in the prior 2 months (51 versus 5.8%), highlighting the possibility of delayed diagnoses and missed opportunities for prevention.
of 291 acutely head-injured children less than 3-years old admitted to 14 pediatric ICUs (PICUs) in the Pediatric Brain Injury Research Network. The rule included four variables: acute respiratory compromise any time prior to admission; bruising of the ears, neck, or torso; bilateral or interhemispheric subdural hemorrhages or fluid collections; and any skull fractures aside from isolated, unilateral, nondiastatic, linear, and parietal fractures. In this validation population, which excluded children injured in motor vehicle accidents and those with preexisting brain conditions, presenting with one or more of the four variables carried a sensitivity of 96% and a specificity of 43% for AHT in comparison to a priori definitional criteria for AHT and identified 98% of the 144 children ultimately diagnosed with AHT. According to the authors, this screening rule is meant to capture nearly all children who should undergo further diagnostic evaluation for potential abuse. Historical clues, such as denial of accidental or inflicted head trauma, inconsistency of the history with the child’s gross motor skills, or variation in historical details over time, prompted evaluation of the three children with AHT missed by the rule.
Abusive versus accidental head trauma by head injury pattern
As exemplified in a recent case report by Tilak and Pollock [11] from the pediatric emergency medicine literature, patients with AHT may present with seemingly unrelated and nonspecific complaints, making its recognition and diagnosis particularly challenging. The recent literature has made important strides toward strengthening the ability of clinicians to identify AHT.
The body of AHT literature supports an understanding that subdural hemorrhage that is either unexplained or not related to comorbidity [such as macrocrania [14] and increased intracranial pressure (ICP) [15]] warrants raised suspicion for nonaccidental trauma. In an effort to build upon and further clarify this literature, Roach et al. [16 ] retrospectively reviewed the largest case series of AHT to date, 580 young children over the course of 16 years. Patients with AHT were significantly less likely than those with accidental injury to have skull fractures (22 versus 52%) and epidural hematomas (3 versus 11%) and significantly more likely to have diffuse axonal injury (14 versus 8%) and SDH (76 versus 23%). Of course, given that the child protection team likely incorporated head injury pattern into their diagnosis of AHT, it is not possible to avoid circularity of reasoning in these findings. From the emergency medicine perspective, head injury pattern can modify suspicion for AHT and guide the decision about whether or not to seek further expert consultation.
A validated clinical prediction rule among head-injured children
A prospective biomarker for mild abusive head trauma
CLINICAL RECOGNITION
Having previously derived a clinical prediction rule to screen for AHT [12], Hymel et al. [13 ] prospectively validated the rule in a new population &&
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Clinical prediction rules and radiologic findings that distinguish abusive from accidental head trauma rely in large part on the recognition of acute
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head injury. However, given that AHT often presents with nonspecific symptoms, without external sign of injury, and without a disclosed history of head trauma, researchers hope that certain serum biomarkers might help identify more subtle cases of AHT just as transaminases are used to screen for occult abdominal trauma [17]. Gao et al. [18 ] compared serum proteomic profiles of patients diagnosed with mild AHT [Glasgow Coma Scale (GCS) 13–15] who presented for the evaluation of head trauma or a neurologic symptom (e.g., vomiting, fussiness, or seizures) with those of matched controls presenting with similar symptoms but without a history of head trauma or diagnosis of brain injury. Serum amyloid A, an acute phase reactant previously identified as a potential marker of injury in hypoxic-ischemic encephalopathy and traumatic brain injury (TBI), had significantly higher mean expression among AHT cases versus controls, with impressive discriminating ability and an area under the receiver operator curve of 0.96. &&
DIAGNOSTIC WORK-UP According to a recent, comprehensive review by Ryan et al. [19 ] with the American College of Radiology, noncontrast head computed tomography (CT) is indeed the initial study of choice for suspected AHT. Furthermore, in the absence of neuroimaging findings, recent evidence by Greiner et al. [20] supports deferral of dedicated retinal exam. The radiology and ophthalmology literature relating to the diagnosis of AHT continues to grow. &&
Patterns of intracranial injury in abusive head trauma The neuroradiologic finding of hemispheric hypodensity in association with SDH has been previously described in AHT and is known to be associated with poor outcomes [21,22]. Foster et al. [23 ] have attempted to identify clinical risk factors for hemispheric hypodensity in AHT patients with SDH. In their study of 24 children with AHT, 13 developed hemispheric hypodensity. Daily ICP maximums and intensity of ICP monitoring were significantly higher in patients with hemispheric hypodensity than those without hemispheric hypodensity. Hypoxia, hypotension, and cardiopulmonary arrest, need for blood transfusions and daily blood glucose levels, tended to be higher in the hemispheric hypodensity patients, though not significantly so. The underlying pathophysiology of hemispheric hypodensity remains unknown. Sieswerda-Hoogendoorn et al. [24 ] compared 54 AHT victims with impact head trauma, indicated by scalp soft-tissue injury or skull fracture, with 45 AHT victims without clinical &
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evidence of impact. Children with skull fractures had fewer hypoxic-ischemic injuries than those without fractures (33 versus 57%), but there were no other significant differences in neuroradiological or musculoskeletal findings between impact and nonimpact cases, suggesting that the determination of injury mechanism is not straightforward.
Forensic use of neuroimaging Thomas et al. [25] studied 149 patients, less than 2 years of age, with accidental head injury. Many had skull fractures (36%), about one third of whom had thin, underlying SDH. Only two patients had isolated SDH without skull fracture. All patients who had radiologically identified parenchymal injuries, including hypoxic-ischemic, or severe neurologic sequelae had corresponding high-force mechanisms of injury, supporting the dismissal of minor mechanisms of trauma as potential explanations of severe intracranial injuries. CT and MRI have been used forensically in an attempt to determine the age of SDH in possible AHT patients. Sieswerda-Hoogendoorn et al. [26] performed a literature review of 22 studies describing SDHs on CT, and four on MRI, concluding that, at present, evidence does not support using these imaging modalities to determine the age of SDH.
Utility of MRI In addition to the identification of cervical spine injuries and retinal hemorrhages, discussed below, the use of MRI in the diagnosis and prognostication of AHT has an expanding literature base. In their cohort of 74 children less than 36 months with head trauma, Kadom et al. [27 ] found a significant association between bilateral hypoxic-ischemic injury pattern and AHT, hypothesized to be because of injury at the craniocervical junction resulting in apnea and hypoxia [28]. Diffusion MRI is a technique of mapping of the diffusion of molecules in tissues, with low diffusion measurements in the brain signifying tissue damage. Imagawa et al. [29] used diffusion tensor imaging in 17 infants with AHT and 34 control infants of similar postconceptual age who underwent MRI for other indications. Reduced ‘axial diffusivity’ was found widespread in the white matter of AHT patients compared with controls, and was worse in the patients with severe outcomes than mild/moderate outcomes, findings with potential for diagnostic and prognostic applications. &&
Differential diagnosis for retinal hemorrhages It is well known that retinal hemorrhages are encountered in up to 50–100% of children who Volume 27 Number 3 June 2015
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Update on abusive head trauma Shaahinfar et al.
have sustained an abusive head injury [30]; however, retinal hemorrhages are not exclusive to AHT and have previously been reported in other conditions (e.g. [14,15]) with varying prevalence. In a study examining a prospective cohort of over 2000 vaginal births, Laghmari et al. [31 ] reported nearly one third of healthy newborns exhibited retinal hemorrhages. The hemorrhages tended to be few in number and localized to the optic discs and posterior pole of the retina. Furthermore, the majority of the hemorrhages had resolved within 1 week of birth and all had resolved within 4 weeks. In the nonabused critically ill child, a 15% prevalence of retinal hemorrhages has been reported, with more severe, widespread findings rarely occurring [32]. Specifically examining the critically ill intubated child, Longmuir et al. [33] reported an even lower prevalence of retinal hemorrhages; without a history of trauma, diffuse multilayered hemorrhages were not found. Understanding how retinal hemorrhages present in various clinical conditions may influence the need for further AHT investigation. &
Mechanism for retinal injury and standardizing retinal findings As demonstrated in recent experimental models by Yamazaki et al. [34], the primary proposed mechanism for the widespread, multilayered retinal hemorrhages in children who undergo shaking with violent, rotational movements of the eyes, is that the vitreous humor exerts extreme traction on the retina, in contrast with unidirectional/blunt head trauma, which generally results in few or no retinal hemorrhages [35]. Levin et al. [36 ] developed a web-based tool to document the various characteristics of retinal hemorrhages, in an effort to establish a universally accepted standard for recording retinal findings. The investigators reported high interobserver and intraobserver reliability among pediatric ophthalmologists. Zuccoli et al. [37] compared susceptibility weighted MRI to the dilated fundoscopic exam, the gold standard, at identifying retinal hemorrhages. The authors reported an MRI sensitivity of 83%, supporting its potential as a diagnostic tool and its utility when a dilated fundoscopic exam is not possible. In a cohort of children with suspected AHT, Longmuir et al. [38 ] found that a quantitative measurement of the area of retinal hemorrhages was significantly higher in children with axial skeletal fractures, with signs of severe brain trauma on neuroimaging, and with definite versus possible abuse, findings which have potential medicolegal implications.
MANAGEMENT OF NEUROLOGIC INJURY Recent publications in the neurology, orthopedics, and neurosurgery literature have emphasized the importance of early identification and treatment of the immediate neurologic sequelae that can be associated with AHT in infants and young children.
Subclinical seizures and status epilepticus Although clinical seizures are a known complication of AHT, less is known about the prevalence of subclinical seizures in these children. Hasbani et al. [39] conducted a retrospective review of 32 children 2 years of age and younger admitted to the PICU with AHT. Of the 21 patients who underwent electroencephalographic (EEG) monitoring, 12 had electrographic seizures, eight had only nonconvulsive seizures on EEG, and eight experienced electrographic status epilepticus. Though limited by a small sample size, no significant association was detected between the presence of electrographic seizures and either clinical seizures at presentation or abnormalities on neuroimaging. Drawing from a larger, prospective cohort of 87 patients admitted to the PICU for acute, mild to severe TBI who underwent continuous EEG monitoring by protocol, Arndt et al. [40 ] found that younger age, AHT, and intraaxial bleed were risk factors for both status epilepticus and subclinical status epilepticus. Further urging a high index of suspicion for AHT in infants with seizures or status epilepticus, Fernandez-Menendez et al. [41] presented case reports of two young infants who were ultimately diagnosed with AHT after developing status epilepticus in the context of intercurrent febrile respiratory infections. &&
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Associated spinal injuries Aside from vertebral plain films in the skeletal survey, screening for more subtle spinal injuries is not a routine component of the AHT work-up, and two recent retrospective studies would advocate otherwise [27 ,42 ]. Knox et al. [42 ] reviewed all pediatric cases of spinal trauma diagnosed over 9 years at a level 1 trauma center. They found that 11 of 342 (3.2%) cases were caused by nonaccidental trauma and that this was tied with motor vehicle collisions as the most common mechanism among children under age 2. Eight of these children had associated head trauma. Taking a complementary approach, Kadom et al. [27 ] reviewed 74 cases of head trauma in children less than 3 years of age in which the child abuse team became involved and both brain and cervical spine MRI were obtained. Thirty-six percent of patients were found to have cervical spine injuries, which were predominantly
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ligamentous but also included three patients with more severe injuries. Cervical spine injury, although seen in most patients with bilateral hypoxic-ischemic brain injury from AHT, did not distinguish between abusive and accidental head trauma. Given the high incidence of cervical spine injury in children with suspected AHT, the authors argue that its presence may be useful in differentiating between traumatic and atraumatic SDH.
from a nationwide health insurance claim database, Peterson et al. [45 ] contributed significantly to our understanding of costs attributed to AHT. They found that AHT was associated with significantly greater medical service use and higher inpatient, outpatient, drug, and total cost over multiple years. They estimated that the excess cost attributable to AHT over 4 years following diagnosis was $47 952 per patient.
Neurosurgical intervention for traumatic subdural hematoma
Primary prevention of abusive head trauma
There is no standardized protocol for the neurosurgical treatment of traumatic SDH secondary to AHT in children younger than 2 years of age, though potential indications include signs of intracranial hypertension, large hematoma size (e.g. >10 mm), and low GCS (e.g. GCS 12). Melo et al. [43] described their own experiences treating 184 children younger than 2 years admitted to the neurosurgical PICU with traumatic SDH on CT concerning for AHT. Sixty percent underwent emergency neurosurgical intervention. Craniotomy and decompressive craniectomy were only completed in two cases, respectively, all with massive acute SDH and severe intracranial hypertension. Subdural puncture and external subdural drainage proved to provide only transient stabilization in many patients, who commonly required definitive treatment with subdural-peritoneal or subduralsubgaleal shunt.
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Although most of the evidence regarding child abuse prevention centers around secondary prevention for at-risk children through home visiting programs, most publications this year related to AHT have reported on more broadly directed, primary prevention efforts conducted in the clinical setting. Simonnet et al. [46] found that a short talk and pamphlet on infant crying and AHT during 190 routine newborn examinations was feasible, acceptable, and significantly improved parental knowledge. Allen [47 ] conducted a systematic review of 10 similar newborn interventions and described two studies, published in 2005 [48] and 2011 [49], respectively, which were able to demonstrate significant decreases in AHT rate post-intervention. These findings suggest an important opportunity for educational interventions directed toward parents of newborns seen in the ED. &
CONCLUSION PUBLIC HEALTH IMPLICATIONS As with other forms of abuse and neglect, there has been ongoing research to measure the longterm impacts of AHT, which further underscores the need to develop and evaluate effective prevention efforts.
Outcomes and costs of abusive head trauma Risen et al. [44] compared functional outcomes in 28 AHT patients with age-matched and sex-matched controls with non-AHT admitted to the same inpatient rehabilitation unit. Though the two cohorts had similar brain injuries, the AHT group had more associated injuries with the potential for neurologic sequelae, including status epilepticus. Although similar proportions of children greater than 12 months of age in both groups attained independent ambulation and expressive language by time of discharge, significantly fewer children with AHT ultimately achieved these outcomes. Drawing 1209 patients with AHT and 5895 matched controls 312
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AHT is a complex diagnosis, with social, legal, and medical implications, and a 70 year, often contentious history in the medical literature [50]. With this expanding body of literature and the support of future studies, there is hope that clinicians, including those in the ED, may be more and more equipped to accurately and effectively recognize, diagnose, and manage this often occult injury. In light of the sobering costs to these children and the healthcare system, additional resources should be dedicated toward developing and evaluating effective prevention efforts. Acknowledgements None. Financial support and sponsorship None. Conflicts of interest There are no conflicts of interest. Volume 27 Number 3 June 2015
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Update on abusive head trauma Shaahinfar et al.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Duhaime AC, Alario AJ, Lewander WJ, et al. Head injury in very young children: mechanisms, injury types, and ophthalmologic findings in 100 hospitalized patients younger than 2 years of age. Pediatrics 1992; 90:179–185. 2. Billmire ME, Myers PA. Serious head injury in infants: accident or abuse? Pediatrics 1985; 75:340–342. 3. Bruce DA, Zimmerman RA. Shaken impact syndrome. Pediatr Ann 1989; 18:482–484; 486–489, 492–494. 4. Jenny C, Hymel KP, Ritzen A, et al. Analysis of missed cases of abusive head trauma. JAMA 1999; 281:621–626. 5. Caffey J. The whiplash shaken infant syndrome: manual shaking by the extremities with whiplash-induced intracranial and intraocular bleedings, linked with residual permanent brain damage and mental retardation. Pediatrics 1974; 54:396–403. 6. Christian CW, Block R; Committee on Child Abuse and Neglect, American Academy of Pediatrics. Abusive head trauma in infants and children. Pediatrics 2009; 123:1409–1411. 7. Parks SE, Annest JL, Hill HA, Karch DL. Pediatric abusive head trauma: recommended definitions for public health surveillance and research. Atlanta, GA: Centers for Disease Control and Prevention; 2012. pp. 5–16. 8. Shanahan ME, Zolotor AJ, Parrish JW, et al. National, regional, and state abusive head trauma: application of the CDC algorithm. Pediatrics 2013; 132:e1546–e1553. 9. Selassie AW, Borg K, Busch C, Russell WS. Abusive head trauma in young & children: a population-based study. J Trauma Nurs 2014; 21:72–82. This is the first population-based study to use both hospital and ED databases to estimate AHT incidence and determine relevant risk factors, highlighting the need to include ED patients to capture less severe cases of AHT. 10. Ortega HW, Vander Velden H, Kreykes NS, Reid S. Childhood death attributable to trauma: is there a difference between accidental and abusive fatal injuries? J Emerg Med 2013; 45:332–337. 11. Tilak GS, Pollock AN. Missed opportunities in fatal child abuse. Pediatr Emerg Care 2013; 29:685–687. 12. Hymel KP, Willson DF, Boos SC, et al. Derivation of a clinical prediction rule for pediatric abusive head trauma. Pediatr Crit Care Med 2013; 14:210–220. 13. Hymel KP, Armijo-Garcia V, Foster R, et al. Validation of a clinical prediction && rule for pediatric abusive head trauma. Pediatrics 2014; 134:e1537–e1544. Although not obviating the need for clinical reasoning, the authors have validated a highly sensitive clinical prediction rule using four variables readily available at time of admission to the PICU to reliably detect and prompt work-up for potential AHT. Given its high sensitivity and relatively low specificity, the rule is meant to be implemented as a screening tool. 14. Greiner MV, Richards TJ, Care MM, Leach JL. Prevalence of subdural collections in children with macrocrania. AJNR Am J Neuroradiol 2013; 34:2373–2378. 15. Binenbaum G, Rogers DL, Forbes BJ, et al. Patterns of retinal hemorrhage associated with increased intracranial pressure in children. Pediatrics 2013; 132:e430–e434. 16. Roach JP, Acker SN, Bensard DD, et al. Head injury pattern in children can & help differentiate accidental from nonaccidental trauma. Pediatr Surg Int 2014; 30:1103–1106. The largest reported series to date of children with AHT, this retrospective comparative cohort study further supports the present understanding that the presence of SDH or diffuse axonal injury should raise suspicion for AHT, including in children under age 2. 17. Lindberg DM, Shapiro RA, Blood EA, et al., ExSTRA investigators. Utility of hepatic transaminases in children with concern for abuse. Pediatrics 2013; 131:268–275. 18. Gao W, Lu C, Kochanek PM, Berger RP. Serum amyloid A is increased in && children with abusive head trauma: a gel-based proteomic analysis. Pediatr Res 2014; 76:280–286. Addressing the subset of patients who have no history of trauma and would otherwise be easily missed, this is the first study to compare the serum proteomic profile of children with AHT and matched controls without brain injury. The findings suggest that a child with soft neurologic signs such as vomiting, fussiness, or seizures might require head CT to evaluate for head trauma if their serum amyloid A expression is high. 19. Ryan ME, Palasis S, Saigal G, et al. ACR appropriateness criteria head && trauma–child. J Am Coll Radiol 2014; 11:939–947. Updated, evidence-based guidelines by the American College of Radiology to assist physicians in making imaging decisions across various modalities for pediatric head trauma, including suspected nonaccidental head trauma. 20. Greiner MV, Berger RP, Thackeray JD, Lindberg DM; Examining Siblings to Recognize Abuse (ExSTRA) Investigators. Dedicated retinal examination in children evaluated for physical abuse without radiographically identified traumatic brain injury. J Pediatr 2013; 163:527–531.
21. Duhaime AC, Bilaniuk L, Zimmerman R. The ‘‘big black brain’’: radiographic changes after severe inflicted head injury in infancy. J Neurotrauma 1993; 10 (Suppl 1):S59. 22. Duhaime AC, Durham S. Traumatic brain injury in infants: the phenomenon of subdural hemorrhage with hemispheric hypodensity (‘‘Big Black Brain’’). Prog Brain Res 2007; 161:293–302. 23. Foster KA, Recker MJ, Lee PS, et al. Factors associated with hemispheric & hypodensity after subdural hematoma following abusive head trauma in children. J Neurotrauma 2014; 31:1625–1631. This study takes important steps in identifying clinical risk factors for hemispheric hypodensity, a poorly understood and highly fatal complication after SDH in the AHT population. 24. Sieswerda-Hoogendoorn T, Robben SG, Karst WA, et al. Abusive head & trauma: differentiation between impact and nonimpact cases based on neuroimaging findings and skeletal surveys. Eur J Radiol 2014; 83:584– 588. This retrospective study questions whether neuroimaging and skeletal survey findings contribute much beyond external signs of head trauma (including skull fracture) to the determination of whether a case of AHT occurred by impact or nonimpact mechanism. 25. Thomas AG, Hegde SV, Dineen RA, Jaspan T. Patterns of accidental craniocerebral injury occurring in early childhood. Arch Dis Child 2013; 98:787–792. 26. Sieswerda-Hoogendoorn T, Postema FA, Verbaan D, et al. Age determination of subdural hematomas with CT and MRI: a systematic review. Eur J Radiol 2014; 83:1257–1268. 27. Kadom N, Khademian Z, Vezina G, et al. Usefulness of MRI detection of && cervical spine and brain injuries in the evaluation of abusive head trauma. Pediatr Radiol 2014; 44:839–848. The largest cohort of children evaluated for AHT for which the rate of cervical spine soft-tissue injuries was determined, this article adds significantly to the literature regarding the use of MRI in screening for AHT. The findings support the idea that bilateral hypoxic-ischemic injury as well as cervical injury on MRI may help distinguish between abusive and accidental head trauma, depending on the clinical scenario. 28. Geddes JF, Vowles GH, Hackshaw AK, et al. Neuropathology of inflicted head injury in children. II. Microscopic brain injury in infants. Brain 2001; 124:1299–1306. 29. Imagawa KK, Hamilton A, Ceschin R, et al. Characterization of microstructural injury: a novel approach in infant abusive head trauma-initial experience. J Neurotrauma 2014; 31:1632–1638. 30. Binenbaum G, Forbes BJ. The eye in child abuse: key points on retinal hemorrhages and abusive head trauma. Pediatr Radiol 2014; 44 (Suppl 4): 571–577. 31. Laghmari M, Skiker H, Handor H, et al. Birth-related retinal hemorrhages in the & newborn: incidence and relationship with maternal, obstetric and neonatal factors. Prospective study of 2031 cases. J Fr Ophtalmol 2014; 37:313– 319. An exceptionally large, prospective cohort of over 2000 newborns examined for retinal hemorrhages, further supporting typical characteristics of, and risk factors for, birth-related retinal hemorrhages previously described in the literature and highlighting, with greater confidence, that these hemorrhages only very rarely last beyond 1 month of age. 32. Agrawal S, Peters MJ, Adams GG, Pierce CM. Prevalence of retinal hemorrhages in critically ill children. Pediatrics 2012; 129:e1388– e1396. 33. Longmuir SQ, McConnell L, Oral R, et al. Retinal hemorrhages in intubated pediatric intensive care patients. J AAPOS 2014; 18:129–133. 34. Yamazaki J, Yoshida M, Mizunuma H. Experimental analyses of the retinal and subretinal haemorrhages accompanied by shaken baby syndrome/ abusive head trauma using a dummy doll. Injury 2014; 45:1196– 1206. 35. Morad Y, Wygnansky-Jaffe T, Levin AV. Retinal haemorrhage in abusive head trauma. Clin Experiment Ophthalmol 2010; 38:514–520. 36. Levin AV, Cordovez JA, Leiby BE, et al. Retinal hemorrhage in abusive head & trauma: finding a common language. Trans Am Ophthalmol Soc 2014; 112:1–10. This article makes significant progress toward standardizing the description of retinal finding in order to develop a common language for related clinical, educational, and research purposes. 37. Zuccoli G, Panigrahy A, Haldipur A, et al. Susceptibility weighted imaging depicts retinal hemorrhages in abusive head trauma. Neuroradiology 2013; 55:889–893. 38. Longmuir SQ, Oral R, Walz AE, et al. Quantitative measurement of retinal & hemorrhages in suspected victims of child abuse. J AAPOS 2014; 18:529– 533. Adding an additional level of objectivity to the characterization of retinal hemorrhages, this study is the first to demonstrate that semiautomated quantification of retinal hemorrhages correlates with risk factors for, the definitive diagnosis of, and the neurologic injury from AHT. 39. Hasbani DM, Topjian AA, Friess SH, et al. Nonconvulsive electrographic seizures are common in children with abusive head trauma. Pediatr Crit Care Med 2013; 14:709–715.
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45. Peterson C, Xu L, Florence C, et al. The medical cost of abusive head trauma in the United States. Pediatrics 2014; 134:91–99. Using a novel methodology to incorporate both inpatient and outpatient aspects of healthcare costs that victims of AHT endure, the findings of this article may prove powerful in advocating for cost-effective prevention efforts. 46. Simonnet H, Laurent-Vannier A, Yuan W, et al. Parents’ behavior in response to infant crying: abusive head trauma education. Child Abuse Negl 2014; 38:1914–1922. 47. Allen KA. The neonatal nurse’s role in preventing abusive head trauma. Adv & Neonatal Care 2014; 14:336–342. In this systematic review of primary AHT prevention efforts involving neonatal nurses, attention is drawn to two interventions which show scientific promise in decreasing AHT and the potential to be adapted to diverse settings. 48. Dias MS, Smith K, DeGuehery K, et al. Preventing abusive head trauma among infants and young children: a hospital-based, parent education program. Pediatrics 2005; 115:e470–e477. 49. Altman RL, Canter J, Patrick PA, et al. Parent education by maternity nurses and prevention of abusive head trauma. Pediatrics 2011; 128:e1164– e1172. 50. Ingraham FD, Matson DD. Subdural hematoma in infancy. J Pediatr 1944; 24:1–37. &
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