ORIGINAL ARTICLE

Delayed Homicides and the Proximat e Cause

Peter Lin, MD,* and James R. Gill, MD*
Abstract: Delayed homicides result from complications of remote injuries inflicted by the hands of another. The investigation of delayed homicides may be a challenge due to a number of factors including: failure to report the death to the proper authorities, lack of ready and adequate documentation of the original injury and circumstances, and jurisdictional differences between the places of injury and death. The certification of these deaths also requires the demonstration of a pathophysiologic link between the remote injury and death. In sorting through these issues, it is helpful to rely upon the definition of the proximate cause of death. Over a 2-year period in New York City, there were 1211 deaths certified as homicide of which 42 were due to injuries sustained greater than 1 year before death. The survival interval ranged from 1.3 to 43.2 years. The most common immediate causes of death were: infections (22), seizures (7), and intestinal obstructions/hernias (6). Common patterns of complications included infection following a gunshot wound of the spinal cord, seizure disorder due to blunt head trauma, and intestinal obstruction/hernia due to adhesions from an abdominal stab wound. Spinal cord injuries resulted in paraplegia in 14 instances and quadriplegia in 8. The mean survival interval for paraplegics was 20.3 years and 14.8 years for quadriplegics; infections were a frequent immediate cause of death in both groups, particularly infections due to chronic bladder catheterization. The definition of proximate cause originated with civil law cases and was later applied to death certification as the proximate cause of death. The gradual extinction of the year and a day rule for the limitation of bringing homicide charges in delayed deaths may result in more of these deaths going to trial. Medical examiners/coroners must be able to explain the reasoning behind these death certifications and maintain consistent standards for the certification of all delayed deaths due to any injury (homicides, suicides, and accidents). Key Words: forensic pathology, homicide, proximate cause, delayed complications (Am J Forensic Med Pathol 2009;30: 354 357)

investigate and certify. The investigation of delayed homicides may be a challenge due to a number of issues including: failure to report the death to the proper authorities, lack of ready and adequate documentation of the original injury and circumstances, and jurisdictional differences between the place of injury and death. The certification of these deaths also requires a demonstration of a pathophysiologic link between the remote injury and death. The certification of such a death may be particularly problematic for police and prosecutors who may have to prosecute a 20-year-old homicide. In some instances, however, it may be relatively simple if the perpetrator previously had been identified and tried for attempted murder or some degree of assault immediately following the original injury. In some instances, the perpetrator still may be incarcerated for the prior (or other) offense. These delayed homicides reiterate the importance of always determining the proximate cause of death. The proximate cause of death is that which in a natural and continuous sequence, unbroken by any efficient intervening cause, produces the fatality and without which the end result would not have occurred. It must be an etiologically specific disease or injury. Due to a prolonged survival interval, some deaths may not be immediately recognized as due to injury and therefore not reported to the police or medical examiner/ coroner. Clinical physicians often focus on mechanisms and immediate causes when they certify a death. Therefore, there is a risk that some of these delayed homicides may be missed. The treating physician mistakenly may certify the death as bronchopneumonia (natural) and disregard the fact that the patient was ventilatordependent for 5 years due to a gunshot wound of the upper cervical spinal cord. This is a fairly common occurrence in medicolegal death investigation.

MATERIALS AND METHODS

The New York City Office of Chief Medical Examiner investigates all unexpected, violent, and suspicious deaths in New York City. By statute, these deaths must be reported to the Office of Chief Medical Examiner. We reviewed all medical examiner death certificates for all homicides that occurred between January 1, 2005 and December 31, 2006. Over this 2-year period, there were 1211 homicides. In 42 of these, the ultimately lethal injury occurred greater than one year before death. We reviewed the medical examiner records which included the autopsy, toxicology, and in- vestigators reports. One death did not undergo autopsy because the hospital mistakenly certified the death as natural and the remains were buried. The cause of death is defined as the etiologically specific disease and/or injury responsible for initiating the lethal sequence of events (part 1 on the death certificate). A competent cause of death includes the proximate (underlying) cause. Immediate causes are complications of the underlying cause interposed between the proximate cause and fatal result. Mechanisms are etiologically nonspecific alterations in physiology and biochemistry whereby the causes exert their lethal effects (eg, exsanguination).3 Immediate causes and mechanisms are not required to be listed on the death certificate. In some deaths, there may be a contributing condition (part 2) that contributed to death but did not result in the underlying cause listed in part 1. There is no time limit for the proximate cause to result in death. If there is a direct, unbroken, link between a remote injury and

elayed homicides result from complications of remote injuries inflicted by the hands of another. With the current state of emergency medical services and long-term care advances, some life-threatening injuries are not immediately fatal. The morbidity associated with survival, however, may ultimately result in death.1 For death certification purposes, there is no time limit for the interval between the proximate (underlying) cause and death. Even though an injury may have occurred years prior to death, if there is a direct, unbroken link, without an efficient intervening cause, between the initial injury and death, the injury is the proximate cause of death and dictates the manner of death.2 A suspected homicide due to an injury that occurred years before death is often difficult for a medical examiner/coroner to
Manuscript received March 22, 2007; accepted June 4, 2007. From the *Department of Forensic Medicine, New York University School of Medicine, New York, NY; and New York City Office of Chief Medical Examiner, New York, NY. Reprints: James R. Gill, MD, Office of Chief Medical Examiner, 520 First Avenue, New York, NY 10016. E-mail: jgill@ocme.nyc.gov. Copyright 2009 by Lippincott Williams & Wilkins ISSN: 0195-7910/09/3004-0354 DOI: 10.1097/PAF.0b013e3181c1582a

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TABLE 1.

Proximate and Immediate Causes of Death

Immediate Cause Intestinal Obstruction/ Hernia 2 1 4 7

TABLE 3.

Paralysis Survival Intervals

Ventilator Dependent 0 7 4 Decubitus Ulcers 13 (93%) 6 (75%) 2 (29%) Survival Interval in Years (Mean) 8.332 (20.3) 1.831 (14.8) 1.313.5 (7.4)

Type of Paralysis Paraplegia Quadriplegia Hypoxic-ischemic encephalopathy Hemiplegia No paralysis Total

Total 14 8 7

Proximate Cause Gunshot wound Blunt injury Sharp injury Total

Total 27 9 6 42

Infection 19 4 0 23

Seizure 3 4 0 7

Other 3 1 1 5

2 11 42 11

0 0 21

0 0

212.3 (7.1) 1.343.2 (18.4) 1.343.2 (15.7)

TABLE 2.

Immediate Causes of Death

23 7 3 3 10 7 7 5 Intestinal Obstruction/ Hernia 0 1

Infection Bronchopneumonia Urinary tract infection Decubitus ulcer Combination Posttraumatic seizure disorder Intestinal obstruction/hernia Other

Type of Paralysis Paraplegia Quadriplegia encephalopathy

Total 14 8

Infection 12 6

Seizure 0 0

Other 2 1

the immediate cause or mechanism of death, the injury is the proximate cause of death. If there is an efficient intervening cause then the remote injury is not the underlying cause of death. The manner of death is determined from the circumstances and cause of death. The manners of death listed on the United States Standard Certificate of Death include: natural, accident, suicide, homicide, and undetermined.3 In New York City, deaths also may be certified as therapeutic complication.4 The medicolegal definition of homicide is defined as death at the hand of another or death due to the hostile or illegal act of another. 5 Demonstration of the intent to kill is not needed for a homicide interpretation. In addition, the susceptibility or vulnerability of the victim does not absolve the proximate injury. If the injury contributed to death, it will dominate the determination of the manner of death.

eters placed for hemodialysis which resulted from a complication of a gunshot wound, and 2 hemorrhagic complications. One bleeding complication involved a tracheoinnominate artery fistula due to a long standing tracheostomy and the other was a retroperitoneal hemorrhage during anticoagulation therapy for a deep venous thrombosis complicating paraplegia due to a gunshot wound.

RESULTS
There were 42 homicides in which the proximate injury occurred greater than one year before death. The decedents average age was 42.8 years and ranged from 7 to 84 years. There were 34 males and 8 females. The survival interval following the injury ranged from 1.3 to 43.2 years with a mean of 15.7 years. The proximate and immediate causes of death are listed in Table 1. In 6 deaths, there were additional conditions that contributed to the death. These included: hypertensive and atherosclerotic cardiovascular disease, diabetes mellitus, methadone intoxication, and AIDS. The most common immediate cause of death in this series was infection-related and involved 23 deaths (Table 2). Seven deaths were due to small bowel obstructions or incarcerated hernias that were complications of remote injuries. Seven deaths were due to posttraumatic seizures. The 5 other immediate causes included 1 pulmonary embolism, acute and chronic rejection of a liver allograft (transplanted due to a stab wound), an infection complicating cath 2009 Lippincott Williams & Wilkins www.amjforensicmedicine.com | 355

Am J Forensic Med Pathol Volume 30, Number 4, December 2009 There were 29 injuries that resulted in paralysis including 14 paraplegics (2 cervical and 12 thoracic injuries), 8 quadriplegics, 2 hemiplegics, and 7 with hypoxic-ischemic encephalopathies (Table 3). Of 9 people who died with urosepsis, 8 had documented indwell- ing urinary tract catheters and included 5 paraplegics, 2 quadriple- gics, 1 hemiplegic, and 1 hypoxic-ischemic encephalopathy patient. There were 2 quadriplegics who survived over 30 years after the injury. One had required placement of a tracheostomy 4 weeks before death due to infectious complications. The other was not ventilator dependent. The immediate causes of death for the para- lyzed patients are provided in Table 4.

Hemiplegia No paralysis Total

2 11 42

1 1 23

1 4 7

Delayed Homicides

0 5 7

0 1 5

DISCUSSI ON Proximate Cause

The term proximate cause originated in civil law. In 1908, the legal definition of proximate cause was given in the Pawsey versus Scottish Union and Nation decision: Proximate cause means the active, efficient motion that sets in motion a train of events, which brings about a result, without the intervention of any force started and working actively from a new and independent source. Pawsey involved an insurance claim due to a fire in Kingston, Jamaica, following the 1907 Jamaican earthquake. The issue was whether the fire was the result of the earthquake which would have been an exclusion under the insurance policy. The case was appealed to the British Privy Council which agreed with the jury decision that there was reasonable doubt that the fire was started by the earthquake.6 Legally, it has been refined to the initial act that sets off a natural and continuous sequence of events that produces injury. In the absence of the initial act, which produces injury, no injury would have resulted (see also Palsgraf v. Long Island Railroad Co., 162 N.E. 99. N.Y. 1928). In malpractice claims, one element that a plaintiff must establish is that a breach of duty was the proximate cause of the injury. In 1948, the Sixth Decennial International Revision Confer- ence agreed that vital statistics must code the underlying cause of death. 5 They defined the underlying cause of death as: the disease or

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injury that initiated the train of morbid events leading directly to death or the circumstances of the accident or violence, which produced the vital injury. Their design of the new death certificate included separate entries for the cause, manner, and circumstances of death. 7 From this similar terminology, it appears that the medicolegal definition of the proximate cause of death had its origin in the legal definition of proximate cause. In law, a proximate cause is an event sufficiently related to a legally recognizable injury to be held the cause of that injury. The legal use of proximate cause mainly is concerned with torts and the assignment of negligence; however, there are logical similarities with the use of proximate cause of death by the medicolegal field. There are 2 types of causation in the law, cause-in-fact and proxi- mate (or legal) cause. Cause-in-fact is determined by the but-for test: but for the action, the result would not have happened. For example, but for running the red light, the collision would not have occurred. For an act to cause harm, both tests must be met; proximate cause is a legal limitation on cause-in-fact. Since but- for causation is very easy to show and does not assign culpability (but for the snow, you would not have crashed your car), there is a second test used to determine whether an action is close enough to a harm in a chain of events to be a legally culpable cause of the harm. This test is the proximate cause. These tests of causality can be applied for death certification. The critical task in certifying a death following a remote injury is to determine whether the remote injury represents the proximate (underlying) cause of death. A prototypical example is a wheelchairbound paraplegic (due to a remote gunshot wound of the spinal cord) who dies from sepsis due to infected decubitus ulcers. In this example, there are at least 3 injuries that meet the but for test-gunshot wound, paraplegia, and decubitus ulcers-but only the gunshot wound meets the proximate cause test. The search for the proximate cause ends with the determination of the etiologically specific disease or injury.

Delayed Causes

Homicides

and

Immediate

An antiquated English common law rule holds that a death must occur within a year and a day after an assault to be considered a homicide. This rule has occasionally been invoked as a defense in jurisdictions where it had yet to be explicitly revoked (see State of Wisconsin v. Picotte, 2003 WI 42). A US Supreme Court ruling in July 2001 affirmed a State Courts abolishment of the rule (Rogers v. Tennessee, US 99 6218) stating that advances in medical and related science have so undermined the rules useful- ness as to render it without question obsolete. It also was abolished in Great Britain with the Law Reform Act of 1996. The gradual extinction of the year and a day rule for bringing homicide charges in delayed deaths, may result in more of these deaths proceeding to trial. Medical examiners/coroners must be prepared to explain the reasoning behind these death certifications and maintain consistent standards for the certification of all delayed deaths due to any injury (homicides, suicides, and accidents). Medical examiner/coroners have no time limit for the interval between an injury and death to invoke the injury as the proximate cause. Therefore, the potentially long interval that may occur between a traumatic injury and death can complicate the cause of death determination. Common problems include the failure of care providers to recognize and report deaths due to remote traumatic injuries, the difficulty in sorting out a complex sequence of events interposed between the injury and death, and the lack of adequate documentation of the original injury and its circumstances. This application of the proximate injury in delayed deaths is not only applied to homicides. Delayed deaths due to injuries regardless of the circumstances (accidents, suicides) also are certified with this method. 356 | www.amjforensicmedicine.com

It is important to note that a medical examiner/coroners determination of homicide as a manner of death is not equivalent to a determination of homicide by a judge or jury. Certification of the manner of death by a medical examiner/coroner is primarily for vital health statistical purposes but also is used by insurance companies and other agencies for internal administrative purposes. The cause of death certification may be more important in subsequent legal proceedings because it requires the gathering of facts obtained through a medicolegal investigation, including an autopsy, and the specialized knowledge to interpret those facts. In criminal trials, the manner of death is ultimately a question for the jury to answer. Nonetheless, the certification of a homicide requires a higher degree of certainty (ie, a reasonable degree of medical certainty) than natural deaths or accidents (a preponderance of the evidence).5 In deaths due to recent injury, it usually is not difficult to meet this higher standard since the mechanism of death (eg, exsanguination) is clearly linked to the injury. When trauma kills so quickly that there is no time for sequelae to develop, the injury is both the immediate and proximate cause of death. 8 In delayed deaths, there typically is an interposing immediate cause. These immediate causes (bronchopneumonia, urosepsis) may result from natural diseases as well as consequences of injury. Therefore, in these delayed deaths, one must link the death to the immediate cause and link the immediate cause to the remote injury. Both links must be made to a reasonable degree of medical certainty to certify the death as a homicide. This higher standard may be difficult to meet in some instances of delayed death and typically requires a diligent review of available records and an autopsy (particularly if competing or contributing conditions unrelated to the remote injury are a concern). The cause of death may be affected by the detection of other noninjury-related comorbidities. The incidence of life-threatening, cardiovascular disease increases with increasing age. In our series, 10 decedents were over 60 years of age and there were some deaths in which coexisting natural disease made a contribution to the death. The decision to include these contributing conditions depends upon a careful review of the circumstances and autopsy findings. The 3 questions that arise with concurrent natural disease are: (1) is the comorbidity to the extent that it is an efficient intervening cause of death? (2) Did the comorbidity contribute to the death in conjunction with the remote injury? (3) If so, was it a major or minor factor? Contrariwise, if the remote injury contributes at all to the death, then the injury will dominate the manner of death determination. For example, one delayed homicide was certified as cardiac arrest due to hypertensive disease (in part 1). This death occurred during emergent surgery for an incarcerated incisional hernia due to a remote repair of a stab wound, which was listed as a contributing condition (part 2). The manner was certified as homicide. There is a potential for obfuscation or confusion with the immediate cause. Particularly in legal proceedings, a party may attempt to blame the death on the immediate cause, ignore the proximate cause of death, or focus on comorbidities. In some instances, there may be an attempt to shift the blame to the caretakers who did not adequately care for the patient. These diversions usually can be addressed by the simple fact that this person would not have died at this time from this complication if the original injury had not occurred. The patient would not have re- quired an indwelling urinary catheter or developed a decubitus ulcer if there was no initial injury. It has been said that the constitution does not guarantee an assailant the right to a healthy victim nor to a doctor who knows how to fix a broken leg. As Adelson noted: If a wound not necessarily fatal, leads to the development of septic or other complications which terminate fatally, the person causing such a wound is responsible for the death as though the wound he inflicted were necessarily fatal. Nor will the fact that the victim 2009 Lippincott Williams & Wilkins

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might have recovered had a neglected wound been properly treated relieve an assailant of responsibility for causing the death if the original injury was feloniously inflicted.8 Contrariwise, if a wound is not mortal and death results from an independent cause, then this is an example of an efficient intervening cause and the death would not be certified as homicide.8 The morbidity and mortality associated with both paraplegia and quadriplegia are well described in the medical literature.9,10 Studies on paraplegics and quadriplegics have demonstrated longterm survival. A study of nonventilator-dependent patients who survived a traumatic spinal cord injury (without concurrent moderate or severe brain injury) incurred between 25 and 34 years of age in Ontario, had a median survival of 38 years postinjury. 10 They also found a difference in the median survival time for paraplegics and quadriplegics (41 vs. 32 years postinjury). Factors that affect mortality include age at the time of injury and year of injury. Injury at younger ages experience better survival outcomes and, due to treatment improvements, injuries that occurred after the early 1970s also have a decreased mortality. There have been conflicting data on whether the vertebral level of injury predicts mortality. 10 A study in Great Britain examined long-term survival in over 3000 individuals with spinal cord injuries that occurred over a 50-year period.9 They found the top 3 causes of death were: pulmonary infection, urinary system complications, and heart disease. Men were 75% more likely than women to die of urinary system disease. Our data show a high number of infection deaths in the patients with paralysis. Decreased ambulation affects many aspects of the body including the cardiopulmonary system (deconditioning 11), skin integrity, and genitourinary dysfunction with the chronic need for bladder catheterization. Infections due to chronic bladder catheterization are a well-described complication in patients with spinal cord injuries.1215 Posttraumatic seizures are a well recognized complication of brain injury. 16 19 Posttraumatic seizures are categorized as early (within one week of the injury) and late (after 1 week). Annegers et al studied over 4500 children and adults with traumatic brain injury. 16 They found significant risk factors for later seizures in- cluded brain contusion with subdural hematoma, skull fracture, loss of consciousness or amnesia for more than 1 day, and an age of 65 years or older. Seizures following penetrating war injuries also have been reported. 19 The risk of posttraumatic seizures after severe head injury is 7.1% within the first year and 11.5% within 5 years.18 Approximately 5.5% of all patients with a diagnosis of epilepsy have a history of head trauma and the incidence of having at least one late seizure in patients treated for a head injury is about 2%. 17,18 The risk of developing posttraumatic seizures extends for years following the injury with approximately 50% occurring within the first year after the injury.19 In summary, this is a series of 42 delayed homicides over a 2-year period in a large metropolitan medical examiner jurisdiction. To our knowledge, a previous series of delayed homicides has not been reported. Common scenarios of delayed homicides include: infected decubitus ulcers, bronchopneumonia, and urosepsis due to

paralysis following gunshot wounds of the spinal cord; seizures following blunt head injuries; and small bowel incarceration/hernia following stab wounds. In making consistent and accurate cause of death determinations in delayed homicides, it is important to rely upon the definition of proximate cause of death. REFERENCES
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