Failure to Autopsy: The Otto Warmbier Case

Coroner and medical examiner offi ces are charged with the medicolegal investigation of deaths to determine the cause and manner of death. We describe the recent high-profi le case of Otto Warmbier, who tragically died shortly after his return in a coma from North Korea and in which the coroner failed to conduct a complete autopsy, and failed to satisfy the needs of the local, national, and international communities. Medico legal death investigation offi ces, including both medical examiner and coroner offi ces, have a legal responsibility and duty to investigate deaths in the public interest for public safety and public health purposes. Although, they serve the families of the deceased as they can, their raison d’être and priority is service to the greater public good. Thus, they may conduct investigations and even autopsies over the objections of the nextof-kin. Full investigations include a complete forensic autopsy. The utilitarian public interest should, within the constraints of the offi ce resources, drive the decision of whether to autopsy or not. Failure to autopsy can sometimes constitute a breach of faith that the public entrusts in these offi ces. Empirically, this seems to be a greater problem in coroner jurisdictions than in medical examiner offi ces. Specifi cally, we believe the recent case of Otto Warmbier is such a case. Case Report Failure to Autopsy: The Otto Warmbier Case Steven A Koehler1* and Victor W Weedn2 1Former Chief Forensic Epidemiologist at the Allegheny County Medical Examiner’s Offi ce, Pittsburgh Pa. Director: Forensic Medical Investigations, Pittsburgh, PA, USA 2George Washington University, Department of Forensic Sciences, USA *Address for Correspondence: Steven A Koehler, Former Chief Forensic Epidemiologist at the Allegheny County Medical Examiner’s Offi ce, Pittsburgh Pa. Director: Forensic Medical Investigations, Pittsburgh, PA, USA, Tel: 412-4872531; Email: sakoehler100@hotmail.com Submitted: 11 December 2017 Approved: 26 December 2017 Published: 27 December 2017 Copyright: 2017 Koehler SA, et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

The UCMC doctors reported that he was stable but had contractures of his extremities and was in a state of unresponsive wakefulness or persistent vegetative state, in which the brain stem continues to function, but without conscious brain function [10][11][12]. Brain scans revealed Warmbier had suffered extensive loss of brain tissue throughout his brain, consistent with a cardiopulmonary event that caused global anoxia, although they stated that they did not know what caused the cardiac arrest. North Korean medical records and magnetic resonance imaging (MRI) brain scans sent with Warmbier documented extensive brain injury dating back to at least April, 2016 [13]. The UCMC doctors declared that they could ind no evidence of active botulism and that radiologic imaging failed to locate evidence of acute or healing fractures or other evidence of trauma (speci ically noting that there was no injury of the neck). On June 19, 2017, six days after being returned to the U.S., he was pronounced dead in the hospital at 2:20 am.
Reactions to his death were strong [14]. Senator John McCain called it murder. Senator Ben Cardin said, "Otto is dead because of Kim Jong-Il's repressive, murderous regime." Defense Secretary James Mattis said that his death after such a minor infraction, "goes beyond any kind of understanding of law and order, of humanity, of responsibility towards any human being" [12]. North Korean of icials responded that their treatment of him was "humanitarian" despite his being a criminal and enemy of the state, that his death was a mystery, and that their country was a victim of a smear campaign [15].
The Hamilton County Coroner's Of ice in Ohio took possession of the body from the hospital. Otto Warmbier's family asked Dr. Lakshmi Sammarco, a neuroradiologist and the elected coroner, not to perform a complete autopsy, but rather merely to conduct an external inspection of the body [3,[16][17][18]. The family did not offer a reason for their objection [19,20]. The of ice announced that the cause and manner of death were "pending", while waiting for medical records, images, air ambulance records, and interviews with the medical team that treated Warmbier. Otto Warmbier was buried on June 22, 2017 [21].
An external examination was conducted on June 19, 2017 at 5:20 PM at the Hamilton County Morgue. The inal autopsy report was releases 4 months after the death on September 28, 2017 [22]. The key features of the examination are shown in table 1.
On September 27, 2017, the Coroner's Of ice held a press conference and announced that they had concluded their investigation and publicly released their report [22]. The coroner certi ied the cause of death as "Complications of chronic anoxic/ischemic encephalopathy due to unknown insult more than a year prior to death" and the manner of death as "Undetermined". Dr. Sammarco responded to questioning that he died after arrival to the U.S. because his feeding tube was removed and ventral feedings were stopped. She also responded to questioning that Warmbier had not been tortured and that, in fact, he had been well cared for as evidenced by the good condition of the skin and lack of decubitus ulcers, given his contractures. The report also declared that there were "Two partially pigmented scars of the left lower leg and foot with multiple additional small scars" and then describes in more detail scars of the neck and lower extremities. Afterwards, Warmbier's father said that his son had been tortured and President Trump tweeted that Warmbier "was tortured beyond belief by North Korea".

Discussion
In commenting on the Warmbier case, Dr. Brian Peterson, President of the National Association of Medical Examiners, stated, "A complete autopsy with a neuropathological examination could reveal numerous causes for brain injury" [4] and Dr. Cyril Wecht declared "it's a terrible mistake not to perform an autopsy" and then, "If you have something that could be anything other than a Natural death, you're obligated to do an autopsy" [4]. In our opinion, the autopsy should have been performed for the following six reasons:

The national and international interests demanded it
The relationship between the United States and the Republic of North Korea at the time was tense. In fact, many considered that North Korea was the single most important issue facing the administration. North Korea had conducted several nuclear tests and ired several missiles. Furthermore, the public rhetoric between Prime Minister Kim Jong Il and President Donald Trump was increasingly tense and bombastic. Given the international rami ications, the fullest investigation was warranted.

Mystery surrounded the death and there was no obvious explanation evident
In this case, a young healthy person was taken custody by North Korea, but was returned comatose and died shortly thereafter. What happened during this time is unknown due to the communication blackout. Although Warmbier clearly suffered extensive brain damage, there was no reason apparent from an external examination or from the medical records that would explain the reason for the brain damage. At the press conference of September 27 th , Dr. Sammarco commented: "One of the frustrating things is the lack of information about what happened to him in North Korea… All we can do is to theorize, and we hate to theorize without science backing us up..." Further investigation was needed.

The history given to explain the death was suspicious
The rationale given by North Korean diplomats for Warmbier's condition was

General
The body is that of a well-developed, well-nourished adult man that weighs 160.5 pounds. The body measures 74.5 inches in length. The body mass index is 20.33 kg/m 2 . The body appears compatible with the stated age of 22 years. The nose shows no remarkable alteration. The lips and gums show a 4 mm nodule extending above the skin at the mucocutaneous margin of the right lower lip medial to a more lateral area of slight tissue retraction with central small pale scar. The teeth are natural and in good repair. The neck is supple, without masses, and the larynx is in the midline. The thorax is well-developed and symmetrical. The breasts are normally developed and symmetrical without palpable masses. The abdomen is relatively fl at. The upper and lower extremities are symmetrical without absence of digits, but there are fl exion contractures of the mid-arms, hands and wrists and extension contractures of the legs and feet and the feet also extend medially.

Identifying Marks and Scars:
There is a small pale scar of the midline dorsal presacral area. There are multiple very small scars of the dorsal chest. There is a round scar just above the sternal notch with mild retraction, consistent with a tracheostomy scar. There are two punctate pale scars overlying the right internal jugular area. There is a small purple scar involving the lower right prepatellar skin and another small purple scar just distal and lateral to the area of the right patella. There is a row of roughly parallel striae distensae over laying the right inguinal crease and proximal right femoral area. There is a small pigmented scar of the ventromedial right med lower leg. There is a large pigmented scar involving the skin of the junction of the left foot and ankle ventrolaterally. There is a large 4.3 x 1.6 inch irregular pigmented scar with paler areas involving the right foot. There is a slightly pigmented transverse somewhat oval scar involving the ventral proximal left upper arm.
Extenal Evidence of Injury Cause of Death: Complications of chronic anoxic/ischemic encephalopathy due to unknown insult more than a year prior to death.
Manner of Death: Undetermined that he had succumbed to botulism and sleeping pills. While botulism could have caused diaphragmatic paralysis and resultant cerebral anoxic damage, there is no other clinical information to support such a diagnosis that has been given. While an overdose of sleeping pills could have caused respiratory depression and resultant cerebral anoxic damage, this would require taking several pills-although it is possible that he hoarded pills and attempted a suicidal overdose. So the given reasons may be plausible, but appear somewhat dubious. It seems odd that two independent explanations are given and both conditions would be dif icult to prove or disprove a year later. Communications from the North Koreans was notoriously unreliable and here they would have a motive to cover-up for any ill deeds, if such were the case. Given the possibility of an unreliable history, further investigation was warranted.

This was a case of possible homicide
It is clearly possible and was suspected by many that the North Koreans did something to Warmbier that resulted in his condition and ultimate demise, justifying a determination of homicide. An accidental or natural manner is also possible. The Coroner's Of ice seems to recognize the possibility of homicide, when they declared the manner of death to be undetermined. Murder investigations demand autopsies.

Suspicions and possible evidence of torture existed
Speculation abounded that Warmbier was tortured by the North Koreans, including by the parents and President Trump. American missionary Kenneth Bae, a former captive of North Korea, reported that torture was common among those imprisoned [23]. It is conceivable that cerebral anoxia could be caused from gagging, perhaps from overly aggressive water-boarding, or even from a pulmonary thromboembolus resulting from being strapped to a chair for a prolonged period of time. Furthermore, the inding of scars (particularly the 4.3x1.6 inch scar of the right foot dorsum), although not considered to be from torture by the coroner's of ice, should have triggered a suspicion of such and an autopsy should have been conducted to further explore the possibility. Torture is sometimes performed in a way to speci ically avoid external injury, but may still show internal injury upon dissection. Any evidence of torture, whether resulting in death or not, would have been of great interest to the family, the U.S., and the international community as a human rights violation [24].
International law irmly establishes a right to be free of torture. The Universal Declaration of Human Rights; the Convention against Torture and Other Cruel, Inhuman or Degrading Treatment or Punishment (UNCAT), and the International Covenant on Civil and Political Rights; all expressly outlaw it. The Democratic People's Republic of Korea is a signatory of only the last. North Korea is also a signatory to the 1949 Geneva Convention and the 1977 Additional Protocols I and II, which includes the Common Article III that bars torture, cruel, inhumane, and degrading treatment during wartime. It is of note that the U.S. Constitution bars cruel and unusual punishment. The Istanbul Protocol [25] is a United Nations manual on the documentation of torture in the living and the Minnesota Protocol (updated in 2016) [26] is a United Nations manual on investigations of unlawful deaths that includes a section on autopsy; guidance on forensic autopsies is given Forensic Autopsy: Manual for Forensic Pathologists, UN Of ice of Drugs and Crime, October 2015. The assumption is that an autopsy should be performed. The Minnesota Protocol clearly states that a forensic investigation including a complete autopsy is legally warranted in cases of death that may have been caused by acts or omission of the State, deaths that occurred when a person was detained by the State, or deaths that occurred where the State may have failed to meet its obligation to protect life [26]. The Protocol also states that the state (Ohio) has a duty to investigate any suspicious death, deaths where reasonable allegations of a potentially unlawful death, or even where it is not alleged or suspected that the State caused the death or unlawfully failed to prevent it [26]. The Protocol outlines the state's legal obligations and standards relating to the forensic investigation. They include the standard autopsy protocol that includes an External and Internal Examination. A key provision of the investigation is that the investigators must be independent of undue in luence, allow to perform their functions without intimidation, hindrance, harassment, or improper in luence [26].
While, forensic pathologist in the U.S. rarely encounter "true" cases of torture they need to understand and interrupt features of torture [24]. Autopsies are the only scienti ic way to provide the cause of death among detainees, death in custody, political prisoners, and, POWs and ascertain the truth behind how injuries associated with acts of torture [24,[27][28][29][30]. Many methods of torture present with minimal external signs therefore requiring a unique and even more detailed internal examination then a forensic pathology typically conducts [24]. For example injuries to the head and the anterior/posterior regions of the torso are common. However, these types of injuries result on limited or minimal bruising externally therefore, musculocutaneous dissection of these areas is required [24]. A common form of torture is blunt injuries to the soles of the feet, referred to as falanga. Externally this method of torture is normal externally only by dissection of the foot would reveal subcutaneous and subplantar fascical hemorrhage. Injuries to the musculocutaneous system involve the back, buttocks, thigh, and leg also shown minor external signs. Another common type of torture, that of suspension (reverse hanging), can only be con irmed by a dissection of the shoulder joint. Histological examination is an important element of the forensic investigation and injury evaluation. This evaluation will provide timing of the injury and indication of infections [24]. Besides the obligation of the coroner to determine the cause and manner of death the results of the investigation has rami ication if international criminal prosecution charges are procured [24].

The rationale for not conducting the autopsy was insuffi cient
In her press conference of September 27 th , Dr. Sammarco stated: "We felt nothing of signi icance was going to be gained from and autopsy and we honored the family's wishes." The conclusion that nothing would be gained is speculative. She, nor anyone else, knows if an autopsy would have revealed any new indings. It is clear that she thought that a new revelation from the autopsy would be unlikely after a year's time, and perhaps it was, but this should not be left to speculation-the signi icance of the case demanded that we know and the only way to know is to perform the autopsy. She relied on the MRI scans of the head and neck to diagnose anoxic encephalopathy, no trauma to the neck, and no healing or healed fractures of any bones. As a neuroradiologist, she has expertise in reading the MRI scans and would normally rely on her interpretation for clinical patient care. However, MRI scans can be misinterpreted [31] and it is not uncommon for an autopsy to reveal pathology not seen by radiology, even advanced imaging techniques [32]. There was no need to rely on them here, where an autopsy could have been de initive in this regard. Even the more sensitive CT scan is not a substitute to a complete autopsy. A 2007 study examining the correlation between the autopsy and CT as it related to sensitivity, speci icity, and positive predictive values reported sensitivity ranging from 0-75% and overall an inadequate forensic tool for the detection of traumatic injuries (32). Additional studies on post-mortem imaging reported that the cause of death is frequently missed using CT and MRI as a method of cause of the diagnosis or in trauma cases [33,34]. At this point post-mortem imaging is not a subs tuition for the physical autopsy [35].
Finally, she commented that she honored the wishes of the family not to autopsy their son. The public interest, not the private interest of the family, should control the decision here, where the public interest is very strong. Families often initially, while their grieving is fresh, express their desire that an autopsy not be performed, only to later wish an autopsy had been done to answer their questions [36][37][38][39][40].
An autopsy may have disclosed a speci ic etiology to explain a natural death, such as myocardial infarction, arrhythmogenic right ventricular cardiomyopathy, or pulmonary blebs which could have resulted in a spontaneous pneumothorax. Furthermore, traumatic injury, not seen externally would also be important and should have been ruled out to the maximal extent possible. Ultimately, such indings would bear on the manner of death-a ruling of homicide would have had international repercussions and an undetermined manner, as is the case here, seems unsatisfactory.
In a number of high pro ile cases, such as that of Mary Jo Kopechne (traveling with Senator Edward Kennedy) [41,42], Lester Jordan (father of Michael Jordan) [43], and Supreme Court Justice Antonin Scalia [44,45], the failure to perform an autopsy resulted in signi icant speculation at best and failure to accurately ascertain the cause of death and the manner of death at worst. In the case of Kopechne, a lay Pennsylvania judge was moved by the family's desire not to disturb her burial, after Massachusetts medical examiners learned of the death and pressed for an exhumation and autopsy; the latter two cases were decisions of a coroner and a justice-of-peace acting as a coroner.
Coroners appear to be more likely to capitulate to families desires not to do an autopsy than medical examiners. Autopsy rates for coroner jurisdictions are generally lower than for medical examiner of ices. Most coroners are elected and are more sensitive to the desires of their citizen constituents. As mentioned above, families will commonly not want an autopsy initially; but later will regret not having the answers, peace of mind, and closure that an autopsy can provide. Because coroners often serve smaller counties, there are repercussions to their decisions and actions within their communities, beyond non-reelection. On the other hand, medical examiner of ices, headed by appointed forensic pathologists, see their jobs as providing scienti ically and medically accurate determinations of causes and manners of death. Thus, medicolegal death investigation is more likely to be politicized in coroner jurisdictions than in Medical Examiner Of ices.
In Ohio, the coroner is elected every four years and, unlike in most states must be a physician, however, the coroner is not required to be a forensic pathologist-but instead can be any licensed physician regardless of their knowledge of medicolegal death investigation. In this case, Dr. Sammarco was appointed by the Hamilton County Democratic Party's Central Committee in 2012 [46], after the previous coroner died unexpectedly in of ice, and then later elected to coroner in 2013 without any previous experience in medicolegal death investigation [47].
Coroners may feel that they need to ind a balance between the feelings of the nextof-kin and the roles and duties of the coroner's of ice, but this is a misguided premise. Those charged with the responsibility of determining the cause and manner of death have a duty not only to the decedent and the family of the decedent, but also to the community they serve to conduct a complete and through investigation. The coroner or medical examiner must speak for the dead. The postmortem examination represents the inal examination of the body to determine the true cause of death. Their duty to ascertain the cause and manner of death is paramount and should supersede other considerations. Those medicolegal death investigation authorities failing to execute their duties may result in murders going undetected, leave questions unanswered, and fuel rumors and conspiracy theories. The Otto Warmbier case is unfortunately among the latest examples of failure to fully execute the duty to ascertain the cause and manner of death of individuals dying under their jurisdiction.
In summary this case exempli ies not only the main weaknesses of the Coroner's system but also illustrates that even within a Medical Examiner's of ice with their legal authority they can fail to perform their responsibility to conduct a complete and thorough postmortem examination. In this case the medical examiner capitulated to the wishes of the next-of-kin resulting in failure to ascertain the true cause and manner of death, put to rest rumors and conspiracies, and to provide forensic data about a possible torture of an American citizen.