- Email: [email protected]
Mimics of child abuse: Can choking explain abusive head trauma?
Journal of Forensic and Legal Medicine 35 (2015) 33e37
Contents lists available at ScienceDirect
Journal of Forensic and Legal Medicine j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / j fl m
Case review
Mimics of child abuse: Can choking explain abusive head trauma? George A. Edwards* Dell Children's Medical Center, Department of Pediatrics, UT, Austin, Dell Medical School, 4900 Mueller Blvd, Austin, TX 78723, USA
a r t i c l e i n f o
a b s t r a c t
Article history: Received 9 December 2014 Received in revised form 29 April 2015 Accepted 13 June 2015 Available online 3 July 2015
Choking is one of the alternative explanations of abusive head trauma in children that have been offered in courtroom testimony and in the media. Most of these explanations d including choking d are not scientifically supported. This article highlights four points. (1) The origins of choking as an explanation for intracranial and retinal hemorrhages are speculative. (2) Choking has been used in high profile court testimony as an explanation for the death of a child thought to have been abused. (3) A case report that proposes choking as an alternative explanation for the death of a child diagnosed with abusive head trauma includes omissions and misrepresentations of facts. (4) There was a decision by the editor of the journal that published the case report that it was not necessary to include all the facts of the case; moreover, the editor indicated that facts are not required when presenting an alternative explanation. The use of scientifically unsupported alternative explanations for abusive head trauma based on inaccurate and biased information constitutes further victimization of the abused child and represents a travesty of justice. © 2015 Elsevier Ltd and Faculty of Forensic and Legal Medicine. All rights reserved.
Keywords: Abusive head trauma Choking Misinformation Child abuse
1. Introduction Although there is consensus in the medical child abuse community around the scientific basis of diagnosing child abuse and abusive head trauma, controversies persist in the courtroom and beyond.1,2 These controversies are related at least in part to the adversarial nature of the legal system, but they have been magnified by scientifically unsupported assertions offered to explain inflicted injuries.3 Courts rely on physicians' testimony to reach legal decisions. Misleading testimony about unsupported hypotheses generates misunderstanding in the courtroom and obscures the public's understanding of accepted scientific findings. Some physicians have put forward alternative explanations for findings of abusive head trauma that are said to mimic child abuse. These include choking,4 dysphagia,5 vomiting,6 rebleeding of preexisting subdurals from birth,7 vaccinations,8 venous thrombosis,9 and others. While there are legitimate alternative explanations for some of the findings of abusive head trauma, many alternative explanations, including choking, are speculative and not scientifically supported.
* Tel.: þ1 512 324 0165. E-mail address: [email protected].
Choking is an important cause of morbidity and mortality in young children. Injury and death from choking result primarily from food, coins, and toys.10 Aspiration of food or a foreign body can result in airway obstruction. Children with neuromuscular disorders or anatomic abnormalities of the airway may be at greater risk of aspiration. When food causes choking and asphyxiation, the types of food include hot dogs, candy, nuts, and grapes.11 Evidence that milk or formula causes choking with asphyxia or sudden death in previously normal children is lacking. The concept that choking in children results in subdural hemorrhage, extensive retinal bleeding, brain injury, and even death is not based on scientific evidence. This article highlights four points: 1) how the origins of choking as an explanation for abusive head trauma were speculative; 2) how choking has been used in a high profile, controversial case as a courtroom argument to try to explain abusive head trauma; 3) how a published case report that supports the choking argument contains both omissions and misrepresentations of fact; and 4) how an editorial decision allowed the publication of inaccuracies. 2. The origins of choking to explain abusive injuries Some authors have speculated that increased vascular pressure from coughing and/or choking might explain subdural and retinal hemorrhages. Talbert hypothesized that “paroxysmal cough injury”
http://dx.doi.org/10.1016/j.jflm.2015.06.012 1752-928X/© 2015 Elsevier Ltd and Faculty of Forensic and Legal Medicine. All rights reserved.
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G.A. Edwards / Journal of Forensic and Legal Medicine 35 (2015) 33e37
could result in excessive intraluminal pressure causing vascular rupture and that rupture of vessels in the head might result in subdural and retinal hemorrhages.12 Subsequently, Geddes and Talbert used computer modeling to suggest that paroxysmal coughing could account for retinal and subdural bleeding as a result of very high intraluminal pressures that damaged veins. It was pointed out that a history of vomiting, coughing, or choking was not uncommon in otherwise normal infants who had subdural and retinal hemorrhage.13 Citing a case report of a child fatality where the father was convicted of manslaughter, Talbert went on to suggest that dysphagia could be related to subdural hemorrhage, retinal hemorrhage, and death through high intracranial vascular pressures transmitted from intrathoracic pressure.5 Talbert coined the term “Dysphagic Infant Death Syndrome” which he indicated was “consistent with intracranial venous hypertension resulting from feed aspiration, such as violent coughing, or high intrathoracic pressures necessary in attempted cardio-pulmonary resuscitation following apnea.”14 He has also suggested that elevated intraabdominal pressure from the vomiting of pyloric stenosis may cause subdural hemorrhage.15 Despite these speculative articles, autopsy studies in both children and adults who died after choking on food have revealed no evidence of an association between choking and intracranial bleeding.11,16e19 Valsalva retinopathy has been described in adults and adolescents secondary to rapid rise in intra-abdominal and intrathoracic pressure from coughing, vomiting, and weight lifting, but it has not been described in infants. Forceful vomiting in infants from pyloric stenosis does not result in retinal hemorrhages.20 Severe persistent cough in infants has not been associated with retinal hemorrhages.21 Similarly evidence is lacking that pertussis infection results in retinal hemorrhages.22 3. Choking used to explain a high profile death Arguments that coughing or choking could raise venous pressure sufficiently to cause subdural bleeding, subarachnoid bleeding, and even death emerged in testimony in a high profile legal proceeding in 2008. In 1996, Audrey Edmunds was convicted of first-degree reckless homicide for the death of seven month-old Natalie Beard. The child died in Edmunds' care and was found to have cerebral edema, subdural hemorrhage, subarachnoid hemorrhage, and retinal hemorrhages with retinoschisis. Edmunds petitioned unsuccessfully for a new trial, and in 2008 her attorneys appealed the previous denial of a new trial. During the appeals process, several physicians testified as expert witnesses in support of Edmunds' motion. Three of those witnesses testified that choking might have caused Natalie Beard's death.23 Patrick D. Barnes testified that there was a differential diagnosis of possible alternative explanations to explain the child's death that included choking. He testified that coughing or vomiting might cause a re-bleed of an old subdural hematoma. When he was asked whether pressure, such as coughing or vomiting, could cause a rebleed, he testified, “Pressure transmitted with regard e through the veins, like high blood pressure within the veins from the chest certainly can be transmitted there and be associated with choking, vomiting, respiratory problems, yes.” He was then asked, “So choking itself could cause a re-bleed of an old hematoma?” Barnes replied, “Yes. We see it in other conditions in children … children with cardiac problems who have these elevated venous pressures transmitted from the veins around the heart to the brain, and they can bleed and even clot those veins.”23 Barnes also testified that aspiration from a choking episode or an “acute life threatening event” may have been a factor in Natalie Beard's death. John G. Galaznik also testified that choking might have caused Natalie Beard's death. He stated that “micro-aspirations of formula
or liquids can set up laryngospasm and bronchospasm and that aspiration in that situation can result in sudden death.”23 To support this testimony, Galaznik referred to a brief review article.24 Although that article indicates that microaspiration can cause laryngospasm and bronchospasm and that aspiration can be silent with subtle symptoms, it does not support the notion that microaspiration can result in unexpected death with intracranial and retinal hemorrhage. Nothing in the reference provides evidence that aspiration results in elevated intracranial venous pressure that causes cerebral edema, subdural hemorrhages, subarachnoid hemorrhages, retinal hemorrhages or unexpected death. Horace B. Gardner also mentioned choking in his testimony. He stated, “She coughed and choked. She bled in her head.”23 The court eventually ruled to allow Edmunds a new trial. Although it is not known how the court weighed the specific testimony about choking, a speculative, scientifically unsupported concept had been presented in the courtroom to explain the findings of abusive head trauma.
4. Omission and misrepresentation to support choking The same physicians (Barnes, Galaznik, and Gardner) who offered testimony that choking could result in the findings of abusive head trauma in the Edmunds appeal were co-authors of a case report4 that supported choking as an alternative explanation to abusive head trauma. Although the authors did not disclose their source of information or their role as expert witnesses for the defense in the criminal trial that arose from the child's death, there is unequivocal evidence that the report was based on the Zavion Thomas, Jr. case from Austin, Texas. Both the child in the case report and the patient in Austin died at four months of age. When admitted to the hospital, both had identical initial laboratory data (Fig. 1). Identical images to those included in the case report can be found in the imaging findings of the child from Austin, as illustrated in Fig. 2. Additionally the first author of the case report (Barnes) provided sworn testimony during a criminal trial in 2011 in Washington State regarding the source of the case report.25 The following exchange between the prosecutor and Dr. Barnes occurred then: Q. …you and three other doctors have written the only single case report about dysphagic choking; is that right? A. I think that may be correct in terms of imaging findings. Q. Okay. Now, was that a child you actually saw at Stanford? A. No, that was a child abuse case from the State of Texas. Q. And you and the other three doctors in that case were hired by the defense; is that right? A. That is correct. Q. Did you say that anywhere in your article? A. No… Clearly the case report was based on the child who died in Austin, Texas. Nevertheless, the report contained omissions and misrepresentations of the facts of the case.
Fig. 1. Identical initial laboratory results: Austin, TX case vs. Barnes et al. case report.
G.A. Edwards / Journal of Forensic and Legal Medicine 35 (2015) 33e37
Fig. 2. Identical images: Barnes et al. case report (left) vs Austin TX case (right).
Four month-old Zavion Thomas, Jr., for whom this author provided consultation, died as a result of abusive head trauma in May 2006 in Austin, Texas. He had rib fractures in different stages of healing, diffuse brain swelling, bilateral subdural hemorrhages, subarachnoid hemorrhages, cerebellar herniation, diffuse swelling of the cervical spinal cord, and extensive bilateral retinal hemorrhages with bilateral retinoschisis and detachments as well as hemorrhage into the posterior third of both orbits. The child's biological father was convicted of serious bodily injury to a child and sentenced to 55 years in prison.26 His conviction was upheld on appeal.27 The case report did not accurately depict the events leading up to the child's hospital admission. It stated there was a “history of infantile dysphagic choking as consistently provided by the caretaker.”4 It also stated that the father called 911 before taking the child to a neighbor's home. In fact, while the father mentioned choking to providers at the hospital, he did not do so in his extended interview with police. Further, the father never called 911. He first called the mother to tell her the baby was not moving. She told him to call 911. He made a second call to her and a third call to their roommate before taking the baby to a neighbor's home. The neighbor started CPR, and the neighbor's child called 911. Phone records indicated that approximately 20 min elapsed between the first call to the mother and the call to 911. When the police arrived at the child's home, they found marijuana on the floor near a dirty diaper.27 The case report also omitted the fact that the child had a healing rib fracture. In fact, the child had a healing rib fracture with callus formation of the right lateral seventh rib, in addition to three recent rib fractures. The authors were aware of the omission of the healing rib fracture, as Barnes acknowledged it in his testimony at trial. He testified, “There is one rib fracture that is older.” He went on to state regarding the older rib fracture, “and that can certainly date back to birth.”26 Although rib fractures have a higher probability of being abusive than all other skeletal injuries in young children,28 they have been reported very rarely as a result of birth trauma.29e33 Van Rijn et al.33 reported on four cases of birth-related rib fractures and reviewed an additional nine from the literature. All thirteen neonates with birth-related rib fractures had been delivered vaginally. Therefore, there is reason to believe that rib fractures after C-sections are very unlikely. This child had been delivered by C-section. The case report misrepresented the pediatric ophthalmologist's findings. Although there were bilateral retinoschisis and retinal
35
detachments, the authors mentioned only “extensive bilateral RH [retinal hemorrhage] and retinal elevation.”4 They omitted the retinoschisis. The case report misrepresented the child's bleeding. It stated, “Clinically the patient was having bleeding from IV sites and his ears.”4 In fact, he never had any clinically significant bleeding, although he had IV lines, an arterial line, and numerous venipunctures, including femoral and external jugular punctures. The case report suggested that a venous thrombosis played a role in the child's problems. However, the pediatric radiologists and neuroradiologists who reviewed the child's imaging studies saw no evidence of venous thrombosis, and the autopsy found no evidence of venous thrombosis. Furthermore, it is doubtful that any causal relationship exists between intracranial venous thrombosis and subdural hemorrhage in young children.34,35 The case report misrepresented the autopsy findings. It described the autopsy stating, “Although NAI [nonaccidental injury] could not be ruled out, the autopsy findings provided further evidence that the child's injury could result from a dysphagic choking type of acute life threatening event (ALTE) as consistently described by the caregiver.”4 In fact, the autopsy showed a well-healed fracture of the right seventh rib; three recent fractures of the right fifth, sixth, and seventh ribs; marked swelling of the brain; bilateral subdural hemorrhages; subarachnoid hemorrhages; and herniation of the cerebellar tonsils. The Medical Examiner stated, “It is my opinion, based on the investigation of the circumstances and the autopsy findings that the decedent … came to his death as a result of severe closed head injury (shaken baby syndrome).”36 He concluded that the manner of death was homicide. The case report omitted the legal outcome. The authors stated, “The injuries in this case were attributed to shaken baby syndrome before the brain injuries were completely evaluated. The father was charged with fatally shaking the child.”4 In fact, the father was charged with causing serious bodily injury to a child by shaking, impact, and/or both. He was also charged with capital murder. The jury found him guilty of causing serious bodily injury to a child and sentenced him to 55 years in prison. The jury deadlocked on capital murder, and a mistrial was declared on that charge. His subsequent appeal was unsuccessful. In addition to the omissions and misrepresentations, the case report is not consistent with the authors' sworn testimony regarding the cause of the child's death. When the authors testified at the father's trial, they expressed the opinion that the child's death occurred as a result of choking that resulted in hypoxia. They argued that the hypoxia then caused brain damage, disseminated intravascular coagulopathy (DIC), intracranial bleeding, and retinal hemorrhage. They never made reference to increased intrathoracic or vascular pressure from choking. None of the authors used the phrase “dysphagic choking” in their testimony. They explained that hypoxia from choking caused the brain damage and that hypoxia and DIC caused the intracranial and ocular bleeding.26 In contrast, their assessment in the case report was that dysphagic choking caused increased intrathoracic pressure that resulted in increased vascular pressure in the head. They indicated that the increased vascular pressure would cause rupture of blood vessels with resulting subdural, subarachnoid, and retinal hemorrhaging.4 5. Editorial decision After the case report appeared, a letter to the editor was published in the same journal.37 This letter pointed out the omission of the healing rib fracture. In their response to the letter, the authors of the case report ignored this omission.38
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G.A. Edwards / Journal of Forensic and Legal Medicine 35 (2015) 33e37
When physicians, including this author, who had been involved in the care of Zavion Thomas, Jr., became aware that the authors had failed to address an important omission of fact, they wrote an unpublished letter to the editor pointing out further omissions and discrepancies between the actual case and the case report. They requested that the editor retract the case report. The editor declined to do so. His explanation for not retracting the article included the following: This is a case study issue the purpose is to … present an alternative interpretation … This does not require that all the “facts” be presented or even that the presentation stick to the facts of the case at all as it represents, primarily, a vehicle for the presentation of the alternative theory … This is not the presentation of research data and thus the requirement to present all of the data is not appropriate … The presentation is not done as an unbiased interpretation of the data in the first place but rather a demonstration that there can be different interpretations of a given data set … (J. B. Bodensteiner, personal communication, December 2011).
7. Conclusions Abusive head trauma is real; it destroys lives and results in permanent adverse consequences. Testimony to explain deaths and injuries from abusive head trauma with speculative, unsupported alternatives like choking obstructs justice. The use of inaccurate information to try to support speculative explanations is not consistent with scientific standards. Moreover, editorial decisions that do not recognize the importance of adhering to the facts discredit the cause of science and medicine. Finally, denying that a crime against a child victim has occurred results in not only further victimization of the child but also a travesty of justice. Conflict of interest I have no financial or personal relationships that would have influenced this work. I have not received any funding for the work involved in preparing this manuscript. Funding None declared.
The editor's reply confirms his awareness that the case report omitted facts and that interpretation of the data was biased. Since the inaccurate case report was published, it has been cited numerous times.39e43
Ethical approval None declared.
6. Discussion
1. Christian CW, Block R. Abusive head trauma in infants and children. Pediatrics 2009;123(5):1409e11. 2. Hymel KP, Deye K. Abusive head trauma. In: Jenny C, editor. Child abuse and neglect: diagnosis, treatment, and evidence. 1st ed. St. Louis, Missouri: Elsevier/ Saunders; 2011. p. 349e59. 3. Petersen A, Joseph J, Feit M. New directions in child abuse and neglect research. Washington, DC: The National Academies Press; 2014. 4. Barnes PD, Galaznik J, Gardner H, Shuman M. Infant acute life-threatening eventedysphagic choking versus nonaccidental injury. Semin Pediatr Neurol 2010;17(1):7e11. 5. Talbert DG. Dysphagia as a risk factor for sudden unexplained death in infancy. Med Hypotheses 2006;67(4):786e91. 6. Talbert DG. Cyclic vomiting syndrome: contribution to dysphagic infant death. Med Hypotheses 2009;73(4):473e8. 7. Gabaeff SC. Challenging the pathophysiologic connection between subdural hematoma, retinal hemorrhage and shaken baby syndrome. West J Emerg Med 2011;12(2):144e58. 8. Orient JM. Reflections on “shaken baby syndrome”: a case report. J Am Phys Surg 2005;10:45e50. 9. Barnes PD, Krasnokutsky M. Imaging of the central nervous system in suspected or alleged nonaccidental injury, including the mimics. Top Magn Reson Imaging 2007;18(1):53e74. 10. Committee on Injury V, Poison P. Prevention of choking among children. Pediatrics 2010;125(3):601e7. 11. Harris CS, Baker SP, Smith GA, Harris RM. Childhood asphyxiation by food. A national analysis and overview. J Am Med Assoc 1984;251(17):2231e5. 12. Talbert DG. Paroxysmal cough injury, vascular rupture and 'shaken baby syndrome'. Med Hypotheses 2005;64(1):8e13. 13. Geddes JF, Talbert DG. Paroxysmal coughing, subdural and retinal bleeding: a computer modelling approach. Neuropathol Appl Neurobiol 2006;32(6): 625e34. 14. Talbert DG. Shaken baby syndrome: does it exist? Med Hypotheses 2009;72(2): 131e4. 15. Talbert DG. Pyloric stenosis as cause of a venous hypertensive syndrome mimicing true shaken baby syndrome. J Trauma Treat 2011;(1):102. 16. Byard RW. Unexpected death due to acute airway obstruction in daycare centers. Pediatrics 1994;94(1):113e4. 17. Mittleman RE. Fatal choking in infants and children. Am J Forensic Med Pathol 1984;5(3):201e10. 18. Byard RW. Mechanisms of unexpected death in infants and young children following foreign body ingestion. J Forensic Sci 1996;41(3):438e41. 19. Wick R, Gilbert JD, Byard RW. Cafe coronary syndrome-fatal choking on food: an autopsy approach. J Clin Forensic Med 2006;13(3):135e8. 20. Herr S, Pierce MC, Berger RP, Ford H, Pitetti RD. Does valsalva retinopathy occur in infants? an initial investigation in infants with vomiting caused by pyloric stenosis. Pediatrics 2004;113(6):1658e61. 21. Goldman M, Dagan Z, Yair M, Elbaz U, Lahat E, Yair M. Severe cough and retinal hemorrhage in infants and young children. J Pediatr 2006;148(6):835e6. 22. Curcoy AI, Trenchs V, Morales M, Serra A, Pou J. Is pertussis in infants a potential cause of retinal haemorrhages? Arch Dis Child 2012;97(3):239e40. 23. Edmunds Audrey. State of Wisconsin v. 2008. Circuit Court, Dane County.
This analysis allows a comparison of the sworn testimony of defense witnesses who subsequently became the authors of a published case report regarding the death of Zavion Thomas, Jr. The comparison provides a revealing look into the credibility of the authors. They were aware of the omissions made in their case report. They provided one opinion about the cause of the child's death at trial and another in the case report. Choking is not the only scientifically unsupported alternative explanation that has been proposed by one of the authors. Keller and Barnes claimed that vitamin D deficiency explains the findings of skeletal abuse.44 There is substantial evidence, however, that vitamin D deficiency does not explain abusive skeletal injuries.45e48 Furthermore, one of the authors (Barnes) co-authored another case report in Seminars in Pediatric Neurology in 2008 that concluded that a 21 month-old child may have died as a result of an accidental fall instead of abuse.49 Their case report had identical imaging findings with another published case report by Twomey et al. from 2004.50 However, Twomey et al. attributed the child's death to abuse. The report by Barnes et al. also had figures that displayed identical gross and histological findings from the autopsy of a child named Christian Ortiz who died in San Francisco, California in 2003.51 In the 2004 criminal trial that resulted from the death of Christian Ortiz, Barnes provided expert testimony for the defense.52 Barnes did not disclose his role in the trial in his case report. Barnes et al. included Twomey et al. in their references and indicated that Twomey et al. reached their conclusions before the brain and spinal cord injuries were completely evaluated. It should be noted that one of Twomey's co-authors was the medical examiner who performed the child's autopsy; the autopsy report51 had been complete when Twomey et al. submitted their case report. In summary, Barnes' two case reports of 2008 and 2010, both published in the same journal, suggest a pattern of important failures: first, the failure to disclose his role as a defense witness and second, a failure to reveal complete information about the children being described.
References
G.A. Edwards / Journal of Forensic and Legal Medicine 35 (2015) 33e37 24. Mohan P. Aspiration in infants and children. Pediatr Rev 2002;23(9):330e1. 25. Morris Michael. State of Washington v. 2011. Snohomish County. 26. Thomas Zavian. State of Texas v. 2007. Austin, TX: 390th District Court, Travis County, Texas. 27. Zavion Thomas v. State of Texas. 2009. Texas Court of Appeals, 3rd District, Austin, TX. 28. Kemp AM, Dunstan F, Harrison S, Morris S, Mann M, Rolfe K, et al. Patterns of skeletal fractures in child abuse: systematic review. Br Med J 2008;337:a1518. 29. Rizzolo PJ, Coleman PR. Neonatal rib fracture: birth trauma or child abuse? J Fam Pract 1989;29(5):561e3. 30. Barry PW, Hocking MD. Infant rib fractureebirth trauma or non-accidental injury. Arch Dis Child 1993;68(2):250. 31. Hartmann Jr RW. Radiological case of the month. Rib fractures produced by birth trauma. Arch Pediatr Adolesc Med 1997;151(9):947e8. 32. Durani Y, DePiero AD. Images in emergency medicine. Fracture of left clavicle and left posterior rib due to birth trauma. Ann Emerg Med 2006;47(2). 210, 5. 33. van Rijn RR, Bilo RA, Robben SG. Birth-related mid-posterior rib fractures in neonates: a report of three cases (and a possible fourth case) and a review of the literature. Pediatr Radiol 2009;39(1):30e4. 34. McLean LA, Frasier LD, Hedlund GL. Does intracranial venous thrombosis cause subdural hemorrhage in the pediatric population? AJNR Am J Neuroradiol 2012;33(7):1281e4. 35. Kwong Y, Jaspan T. Venous sinus thrombosis and subdural haematomas in infantseis there a causal link? Arch Dis Child 2013;98(8):650e1. 36. Bayardo RJ. Medical examiner report: Zavian Thomas, Jr. Travis County, TX; Office of the Medical Examiner. 2006. 37. Greeley CS. Infant fatality. Semin Pediatr Neurol 2010;17(4):275e8. author reply 9e80. 38. Galaznik J, Barnes PD, Gardner H, Shuman M. Reply to Greeley et al. Semin Pediatr Neurol 2010;17(4):279e80.
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39. Squier W. Retino-dural hemorrhage of infancy. Wiley Encycl Forensic Sci 2013. http://dx.doi.org/10.1002/9780470061589.fsa050.pub2. 40. Goodkin HP. Education of the child neurologist: traumatic brain injury. Semin Pediatr Neurol 2011;18(2):142e4. 41. Choi YJ, Jung MS, Kim SY. Retinal hemorrhage associated with perinatal distress in newborns. Korean J Ophthalmol 2011;25(5):311e6. 42. Romaneli MTdN, Baracat ECE. Evento com aparente risco de morte: uma revis~ ao. Rev Paul Pediatr 2012;30:576e85. 43. van Rijn RR, Spevak MR. Imaging of neonatal child abuse with an emphasis on abusive head trauma. Magnetic Reson imaging Clin N Am 2011;19(4):791e812. viii. 44. Keller KA, Barnes PD. Rickets vs. abuse: a national and international epidemic. Pediatr Radiol 2008;38(11):1210e6. 45. Schilling S, Wood JN, Levine MA, Langdon D, Christian CW. Vitamin D status in abused and nonabused children younger than 2 years old with fractures. Pediatrics 2011;127(5):835e41. 46. Strouse PJ. 'Keller & Barnes' after 5 years-still inadmissible as evidence. Pediatr Radiol 2013;43(11):1423e4. 47. Slovis TL, Strouse PJ, Coley BD, Rigsby CK. The creation of non-disease: an assault on the diagnosis of child abuse. Pediatr Radiol 2012;42(8):903e5. 48. Feldman K. Commentary on “congenital rickets” article. Pediatr Radiol 2009;39(10):1127e9. author reply 30e2. 49. Barnes PD, Krasnokutsky MV, Monson KL, Ophoven J. Traumatic spinal cord injury: accidental versus nonaccidental injury. Semin Pediatr Neurol 2008;15(4):178e84. discussion 85. 50. Twomey EL, Iemsawatdikul K, Stephens BG, Gooding CA. Multiple thoracic vertebral compression fractures caused by non-accidental injury: case report with radiological-pathological correlation. Pediatr Radiol 2004;34(8):665e8. 51. Stephens BG. Medical examiner report: Christian Ortiz. 2003. City and County of San Francisco, California. 52. People v. Mireles, Mario. Court no. 2109324, San Francisco County, California; 2005.
Contents lists available at ScienceDirect
Journal of Forensic and Legal Medicine j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / j fl m
Case review
Mimics of child abuse: Can choking explain abusive head trauma? George A. Edwards* Dell Children's Medical Center, Department of Pediatrics, UT, Austin, Dell Medical School, 4900 Mueller Blvd, Austin, TX 78723, USA
a r t i c l e i n f o
a b s t r a c t
Article history: Received 9 December 2014 Received in revised form 29 April 2015 Accepted 13 June 2015 Available online 3 July 2015
Choking is one of the alternative explanations of abusive head trauma in children that have been offered in courtroom testimony and in the media. Most of these explanations d including choking d are not scientifically supported. This article highlights four points. (1) The origins of choking as an explanation for intracranial and retinal hemorrhages are speculative. (2) Choking has been used in high profile court testimony as an explanation for the death of a child thought to have been abused. (3) A case report that proposes choking as an alternative explanation for the death of a child diagnosed with abusive head trauma includes omissions and misrepresentations of facts. (4) There was a decision by the editor of the journal that published the case report that it was not necessary to include all the facts of the case; moreover, the editor indicated that facts are not required when presenting an alternative explanation. The use of scientifically unsupported alternative explanations for abusive head trauma based on inaccurate and biased information constitutes further victimization of the abused child and represents a travesty of justice. © 2015 Elsevier Ltd and Faculty of Forensic and Legal Medicine. All rights reserved.
Keywords: Abusive head trauma Choking Misinformation Child abuse
1. Introduction Although there is consensus in the medical child abuse community around the scientific basis of diagnosing child abuse and abusive head trauma, controversies persist in the courtroom and beyond.1,2 These controversies are related at least in part to the adversarial nature of the legal system, but they have been magnified by scientifically unsupported assertions offered to explain inflicted injuries.3 Courts rely on physicians' testimony to reach legal decisions. Misleading testimony about unsupported hypotheses generates misunderstanding in the courtroom and obscures the public's understanding of accepted scientific findings. Some physicians have put forward alternative explanations for findings of abusive head trauma that are said to mimic child abuse. These include choking,4 dysphagia,5 vomiting,6 rebleeding of preexisting subdurals from birth,7 vaccinations,8 venous thrombosis,9 and others. While there are legitimate alternative explanations for some of the findings of abusive head trauma, many alternative explanations, including choking, are speculative and not scientifically supported.
* Tel.: þ1 512 324 0165. E-mail address: [email protected].
Choking is an important cause of morbidity and mortality in young children. Injury and death from choking result primarily from food, coins, and toys.10 Aspiration of food or a foreign body can result in airway obstruction. Children with neuromuscular disorders or anatomic abnormalities of the airway may be at greater risk of aspiration. When food causes choking and asphyxiation, the types of food include hot dogs, candy, nuts, and grapes.11 Evidence that milk or formula causes choking with asphyxia or sudden death in previously normal children is lacking. The concept that choking in children results in subdural hemorrhage, extensive retinal bleeding, brain injury, and even death is not based on scientific evidence. This article highlights four points: 1) how the origins of choking as an explanation for abusive head trauma were speculative; 2) how choking has been used in a high profile, controversial case as a courtroom argument to try to explain abusive head trauma; 3) how a published case report that supports the choking argument contains both omissions and misrepresentations of fact; and 4) how an editorial decision allowed the publication of inaccuracies. 2. The origins of choking to explain abusive injuries Some authors have speculated that increased vascular pressure from coughing and/or choking might explain subdural and retinal hemorrhages. Talbert hypothesized that “paroxysmal cough injury”
http://dx.doi.org/10.1016/j.jflm.2015.06.012 1752-928X/© 2015 Elsevier Ltd and Faculty of Forensic and Legal Medicine. All rights reserved.
34
G.A. Edwards / Journal of Forensic and Legal Medicine 35 (2015) 33e37
could result in excessive intraluminal pressure causing vascular rupture and that rupture of vessels in the head might result in subdural and retinal hemorrhages.12 Subsequently, Geddes and Talbert used computer modeling to suggest that paroxysmal coughing could account for retinal and subdural bleeding as a result of very high intraluminal pressures that damaged veins. It was pointed out that a history of vomiting, coughing, or choking was not uncommon in otherwise normal infants who had subdural and retinal hemorrhage.13 Citing a case report of a child fatality where the father was convicted of manslaughter, Talbert went on to suggest that dysphagia could be related to subdural hemorrhage, retinal hemorrhage, and death through high intracranial vascular pressures transmitted from intrathoracic pressure.5 Talbert coined the term “Dysphagic Infant Death Syndrome” which he indicated was “consistent with intracranial venous hypertension resulting from feed aspiration, such as violent coughing, or high intrathoracic pressures necessary in attempted cardio-pulmonary resuscitation following apnea.”14 He has also suggested that elevated intraabdominal pressure from the vomiting of pyloric stenosis may cause subdural hemorrhage.15 Despite these speculative articles, autopsy studies in both children and adults who died after choking on food have revealed no evidence of an association between choking and intracranial bleeding.11,16e19 Valsalva retinopathy has been described in adults and adolescents secondary to rapid rise in intra-abdominal and intrathoracic pressure from coughing, vomiting, and weight lifting, but it has not been described in infants. Forceful vomiting in infants from pyloric stenosis does not result in retinal hemorrhages.20 Severe persistent cough in infants has not been associated with retinal hemorrhages.21 Similarly evidence is lacking that pertussis infection results in retinal hemorrhages.22 3. Choking used to explain a high profile death Arguments that coughing or choking could raise venous pressure sufficiently to cause subdural bleeding, subarachnoid bleeding, and even death emerged in testimony in a high profile legal proceeding in 2008. In 1996, Audrey Edmunds was convicted of first-degree reckless homicide for the death of seven month-old Natalie Beard. The child died in Edmunds' care and was found to have cerebral edema, subdural hemorrhage, subarachnoid hemorrhage, and retinal hemorrhages with retinoschisis. Edmunds petitioned unsuccessfully for a new trial, and in 2008 her attorneys appealed the previous denial of a new trial. During the appeals process, several physicians testified as expert witnesses in support of Edmunds' motion. Three of those witnesses testified that choking might have caused Natalie Beard's death.23 Patrick D. Barnes testified that there was a differential diagnosis of possible alternative explanations to explain the child's death that included choking. He testified that coughing or vomiting might cause a re-bleed of an old subdural hematoma. When he was asked whether pressure, such as coughing or vomiting, could cause a rebleed, he testified, “Pressure transmitted with regard e through the veins, like high blood pressure within the veins from the chest certainly can be transmitted there and be associated with choking, vomiting, respiratory problems, yes.” He was then asked, “So choking itself could cause a re-bleed of an old hematoma?” Barnes replied, “Yes. We see it in other conditions in children … children with cardiac problems who have these elevated venous pressures transmitted from the veins around the heart to the brain, and they can bleed and even clot those veins.”23 Barnes also testified that aspiration from a choking episode or an “acute life threatening event” may have been a factor in Natalie Beard's death. John G. Galaznik also testified that choking might have caused Natalie Beard's death. He stated that “micro-aspirations of formula
or liquids can set up laryngospasm and bronchospasm and that aspiration in that situation can result in sudden death.”23 To support this testimony, Galaznik referred to a brief review article.24 Although that article indicates that microaspiration can cause laryngospasm and bronchospasm and that aspiration can be silent with subtle symptoms, it does not support the notion that microaspiration can result in unexpected death with intracranial and retinal hemorrhage. Nothing in the reference provides evidence that aspiration results in elevated intracranial venous pressure that causes cerebral edema, subdural hemorrhages, subarachnoid hemorrhages, retinal hemorrhages or unexpected death. Horace B. Gardner also mentioned choking in his testimony. He stated, “She coughed and choked. She bled in her head.”23 The court eventually ruled to allow Edmunds a new trial. Although it is not known how the court weighed the specific testimony about choking, a speculative, scientifically unsupported concept had been presented in the courtroom to explain the findings of abusive head trauma.
4. Omission and misrepresentation to support choking The same physicians (Barnes, Galaznik, and Gardner) who offered testimony that choking could result in the findings of abusive head trauma in the Edmunds appeal were co-authors of a case report4 that supported choking as an alternative explanation to abusive head trauma. Although the authors did not disclose their source of information or their role as expert witnesses for the defense in the criminal trial that arose from the child's death, there is unequivocal evidence that the report was based on the Zavion Thomas, Jr. case from Austin, Texas. Both the child in the case report and the patient in Austin died at four months of age. When admitted to the hospital, both had identical initial laboratory data (Fig. 1). Identical images to those included in the case report can be found in the imaging findings of the child from Austin, as illustrated in Fig. 2. Additionally the first author of the case report (Barnes) provided sworn testimony during a criminal trial in 2011 in Washington State regarding the source of the case report.25 The following exchange between the prosecutor and Dr. Barnes occurred then: Q. …you and three other doctors have written the only single case report about dysphagic choking; is that right? A. I think that may be correct in terms of imaging findings. Q. Okay. Now, was that a child you actually saw at Stanford? A. No, that was a child abuse case from the State of Texas. Q. And you and the other three doctors in that case were hired by the defense; is that right? A. That is correct. Q. Did you say that anywhere in your article? A. No… Clearly the case report was based on the child who died in Austin, Texas. Nevertheless, the report contained omissions and misrepresentations of the facts of the case.
Fig. 1. Identical initial laboratory results: Austin, TX case vs. Barnes et al. case report.
G.A. Edwards / Journal of Forensic and Legal Medicine 35 (2015) 33e37
Fig. 2. Identical images: Barnes et al. case report (left) vs Austin TX case (right).
Four month-old Zavion Thomas, Jr., for whom this author provided consultation, died as a result of abusive head trauma in May 2006 in Austin, Texas. He had rib fractures in different stages of healing, diffuse brain swelling, bilateral subdural hemorrhages, subarachnoid hemorrhages, cerebellar herniation, diffuse swelling of the cervical spinal cord, and extensive bilateral retinal hemorrhages with bilateral retinoschisis and detachments as well as hemorrhage into the posterior third of both orbits. The child's biological father was convicted of serious bodily injury to a child and sentenced to 55 years in prison.26 His conviction was upheld on appeal.27 The case report did not accurately depict the events leading up to the child's hospital admission. It stated there was a “history of infantile dysphagic choking as consistently provided by the caretaker.”4 It also stated that the father called 911 before taking the child to a neighbor's home. In fact, while the father mentioned choking to providers at the hospital, he did not do so in his extended interview with police. Further, the father never called 911. He first called the mother to tell her the baby was not moving. She told him to call 911. He made a second call to her and a third call to their roommate before taking the baby to a neighbor's home. The neighbor started CPR, and the neighbor's child called 911. Phone records indicated that approximately 20 min elapsed between the first call to the mother and the call to 911. When the police arrived at the child's home, they found marijuana on the floor near a dirty diaper.27 The case report also omitted the fact that the child had a healing rib fracture. In fact, the child had a healing rib fracture with callus formation of the right lateral seventh rib, in addition to three recent rib fractures. The authors were aware of the omission of the healing rib fracture, as Barnes acknowledged it in his testimony at trial. He testified, “There is one rib fracture that is older.” He went on to state regarding the older rib fracture, “and that can certainly date back to birth.”26 Although rib fractures have a higher probability of being abusive than all other skeletal injuries in young children,28 they have been reported very rarely as a result of birth trauma.29e33 Van Rijn et al.33 reported on four cases of birth-related rib fractures and reviewed an additional nine from the literature. All thirteen neonates with birth-related rib fractures had been delivered vaginally. Therefore, there is reason to believe that rib fractures after C-sections are very unlikely. This child had been delivered by C-section. The case report misrepresented the pediatric ophthalmologist's findings. Although there were bilateral retinoschisis and retinal
35
detachments, the authors mentioned only “extensive bilateral RH [retinal hemorrhage] and retinal elevation.”4 They omitted the retinoschisis. The case report misrepresented the child's bleeding. It stated, “Clinically the patient was having bleeding from IV sites and his ears.”4 In fact, he never had any clinically significant bleeding, although he had IV lines, an arterial line, and numerous venipunctures, including femoral and external jugular punctures. The case report suggested that a venous thrombosis played a role in the child's problems. However, the pediatric radiologists and neuroradiologists who reviewed the child's imaging studies saw no evidence of venous thrombosis, and the autopsy found no evidence of venous thrombosis. Furthermore, it is doubtful that any causal relationship exists between intracranial venous thrombosis and subdural hemorrhage in young children.34,35 The case report misrepresented the autopsy findings. It described the autopsy stating, “Although NAI [nonaccidental injury] could not be ruled out, the autopsy findings provided further evidence that the child's injury could result from a dysphagic choking type of acute life threatening event (ALTE) as consistently described by the caregiver.”4 In fact, the autopsy showed a well-healed fracture of the right seventh rib; three recent fractures of the right fifth, sixth, and seventh ribs; marked swelling of the brain; bilateral subdural hemorrhages; subarachnoid hemorrhages; and herniation of the cerebellar tonsils. The Medical Examiner stated, “It is my opinion, based on the investigation of the circumstances and the autopsy findings that the decedent … came to his death as a result of severe closed head injury (shaken baby syndrome).”36 He concluded that the manner of death was homicide. The case report omitted the legal outcome. The authors stated, “The injuries in this case were attributed to shaken baby syndrome before the brain injuries were completely evaluated. The father was charged with fatally shaking the child.”4 In fact, the father was charged with causing serious bodily injury to a child by shaking, impact, and/or both. He was also charged with capital murder. The jury found him guilty of causing serious bodily injury to a child and sentenced him to 55 years in prison. The jury deadlocked on capital murder, and a mistrial was declared on that charge. His subsequent appeal was unsuccessful. In addition to the omissions and misrepresentations, the case report is not consistent with the authors' sworn testimony regarding the cause of the child's death. When the authors testified at the father's trial, they expressed the opinion that the child's death occurred as a result of choking that resulted in hypoxia. They argued that the hypoxia then caused brain damage, disseminated intravascular coagulopathy (DIC), intracranial bleeding, and retinal hemorrhage. They never made reference to increased intrathoracic or vascular pressure from choking. None of the authors used the phrase “dysphagic choking” in their testimony. They explained that hypoxia from choking caused the brain damage and that hypoxia and DIC caused the intracranial and ocular bleeding.26 In contrast, their assessment in the case report was that dysphagic choking caused increased intrathoracic pressure that resulted in increased vascular pressure in the head. They indicated that the increased vascular pressure would cause rupture of blood vessels with resulting subdural, subarachnoid, and retinal hemorrhaging.4 5. Editorial decision After the case report appeared, a letter to the editor was published in the same journal.37 This letter pointed out the omission of the healing rib fracture. In their response to the letter, the authors of the case report ignored this omission.38
36
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When physicians, including this author, who had been involved in the care of Zavion Thomas, Jr., became aware that the authors had failed to address an important omission of fact, they wrote an unpublished letter to the editor pointing out further omissions and discrepancies between the actual case and the case report. They requested that the editor retract the case report. The editor declined to do so. His explanation for not retracting the article included the following: This is a case study issue the purpose is to … present an alternative interpretation … This does not require that all the “facts” be presented or even that the presentation stick to the facts of the case at all as it represents, primarily, a vehicle for the presentation of the alternative theory … This is not the presentation of research data and thus the requirement to present all of the data is not appropriate … The presentation is not done as an unbiased interpretation of the data in the first place but rather a demonstration that there can be different interpretations of a given data set … (J. B. Bodensteiner, personal communication, December 2011).
7. Conclusions Abusive head trauma is real; it destroys lives and results in permanent adverse consequences. Testimony to explain deaths and injuries from abusive head trauma with speculative, unsupported alternatives like choking obstructs justice. The use of inaccurate information to try to support speculative explanations is not consistent with scientific standards. Moreover, editorial decisions that do not recognize the importance of adhering to the facts discredit the cause of science and medicine. Finally, denying that a crime against a child victim has occurred results in not only further victimization of the child but also a travesty of justice. Conflict of interest I have no financial or personal relationships that would have influenced this work. I have not received any funding for the work involved in preparing this manuscript. Funding None declared.
The editor's reply confirms his awareness that the case report omitted facts and that interpretation of the data was biased. Since the inaccurate case report was published, it has been cited numerous times.39e43
Ethical approval None declared.
6. Discussion
1. Christian CW, Block R. Abusive head trauma in infants and children. Pediatrics 2009;123(5):1409e11. 2. Hymel KP, Deye K. Abusive head trauma. In: Jenny C, editor. Child abuse and neglect: diagnosis, treatment, and evidence. 1st ed. St. Louis, Missouri: Elsevier/ Saunders; 2011. p. 349e59. 3. Petersen A, Joseph J, Feit M. New directions in child abuse and neglect research. Washington, DC: The National Academies Press; 2014. 4. Barnes PD, Galaznik J, Gardner H, Shuman M. Infant acute life-threatening eventedysphagic choking versus nonaccidental injury. Semin Pediatr Neurol 2010;17(1):7e11. 5. Talbert DG. Dysphagia as a risk factor for sudden unexplained death in infancy. Med Hypotheses 2006;67(4):786e91. 6. Talbert DG. Cyclic vomiting syndrome: contribution to dysphagic infant death. Med Hypotheses 2009;73(4):473e8. 7. Gabaeff SC. Challenging the pathophysiologic connection between subdural hematoma, retinal hemorrhage and shaken baby syndrome. West J Emerg Med 2011;12(2):144e58. 8. Orient JM. Reflections on “shaken baby syndrome”: a case report. J Am Phys Surg 2005;10:45e50. 9. Barnes PD, Krasnokutsky M. Imaging of the central nervous system in suspected or alleged nonaccidental injury, including the mimics. Top Magn Reson Imaging 2007;18(1):53e74. 10. Committee on Injury V, Poison P. Prevention of choking among children. Pediatrics 2010;125(3):601e7. 11. Harris CS, Baker SP, Smith GA, Harris RM. Childhood asphyxiation by food. A national analysis and overview. J Am Med Assoc 1984;251(17):2231e5. 12. Talbert DG. Paroxysmal cough injury, vascular rupture and 'shaken baby syndrome'. Med Hypotheses 2005;64(1):8e13. 13. Geddes JF, Talbert DG. Paroxysmal coughing, subdural and retinal bleeding: a computer modelling approach. Neuropathol Appl Neurobiol 2006;32(6): 625e34. 14. Talbert DG. Shaken baby syndrome: does it exist? Med Hypotheses 2009;72(2): 131e4. 15. Talbert DG. Pyloric stenosis as cause of a venous hypertensive syndrome mimicing true shaken baby syndrome. J Trauma Treat 2011;(1):102. 16. Byard RW. Unexpected death due to acute airway obstruction in daycare centers. Pediatrics 1994;94(1):113e4. 17. Mittleman RE. Fatal choking in infants and children. Am J Forensic Med Pathol 1984;5(3):201e10. 18. Byard RW. Mechanisms of unexpected death in infants and young children following foreign body ingestion. J Forensic Sci 1996;41(3):438e41. 19. Wick R, Gilbert JD, Byard RW. Cafe coronary syndrome-fatal choking on food: an autopsy approach. J Clin Forensic Med 2006;13(3):135e8. 20. Herr S, Pierce MC, Berger RP, Ford H, Pitetti RD. Does valsalva retinopathy occur in infants? an initial investigation in infants with vomiting caused by pyloric stenosis. Pediatrics 2004;113(6):1658e61. 21. Goldman M, Dagan Z, Yair M, Elbaz U, Lahat E, Yair M. Severe cough and retinal hemorrhage in infants and young children. J Pediatr 2006;148(6):835e6. 22. Curcoy AI, Trenchs V, Morales M, Serra A, Pou J. Is pertussis in infants a potential cause of retinal haemorrhages? Arch Dis Child 2012;97(3):239e40. 23. Edmunds Audrey. State of Wisconsin v. 2008. Circuit Court, Dane County.
This analysis allows a comparison of the sworn testimony of defense witnesses who subsequently became the authors of a published case report regarding the death of Zavion Thomas, Jr. The comparison provides a revealing look into the credibility of the authors. They were aware of the omissions made in their case report. They provided one opinion about the cause of the child's death at trial and another in the case report. Choking is not the only scientifically unsupported alternative explanation that has been proposed by one of the authors. Keller and Barnes claimed that vitamin D deficiency explains the findings of skeletal abuse.44 There is substantial evidence, however, that vitamin D deficiency does not explain abusive skeletal injuries.45e48 Furthermore, one of the authors (Barnes) co-authored another case report in Seminars in Pediatric Neurology in 2008 that concluded that a 21 month-old child may have died as a result of an accidental fall instead of abuse.49 Their case report had identical imaging findings with another published case report by Twomey et al. from 2004.50 However, Twomey et al. attributed the child's death to abuse. The report by Barnes et al. also had figures that displayed identical gross and histological findings from the autopsy of a child named Christian Ortiz who died in San Francisco, California in 2003.51 In the 2004 criminal trial that resulted from the death of Christian Ortiz, Barnes provided expert testimony for the defense.52 Barnes did not disclose his role in the trial in his case report. Barnes et al. included Twomey et al. in their references and indicated that Twomey et al. reached their conclusions before the brain and spinal cord injuries were completely evaluated. It should be noted that one of Twomey's co-authors was the medical examiner who performed the child's autopsy; the autopsy report51 had been complete when Twomey et al. submitted their case report. In summary, Barnes' two case reports of 2008 and 2010, both published in the same journal, suggest a pattern of important failures: first, the failure to disclose his role as a defense witness and second, a failure to reveal complete information about the children being described.
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