Pathology of Asphyxial Death

"Asphyxia" is a term derived from Greek that literally translates as "stopping of the pulse." This term refers to a multi-etiologic set of conditions in which there is inadequate delivery, uptake and/or utilization of oxygen by the body’s tissues/cells, often accompanied by carbon dioxide retention.

Traditionally, the conditions leading to asphyxia have included breathing an oxygen-deficient atmosphere and/or interference with the act of breathing (ie, inhaling and exhaling) and/or respiration (ie, gas exchange and the utilization of oxygen). Conditions that historically were thought to involve airway compromise but are now recognized to involve restriction of blood flow or altered hemodynamics (eg, hanging, strangulation, and compression asphyxia) continue to be classified as asphyxia.

Although many natural disease processes may involve inadequate uptake and/or delivery of oxygen (eg, chronic obstructive pulmonary disease [COPD]), the term "asphyxia" is generally reserved for conditions related to abnormal atmosphere and mechanical and chemical effects directly leading to the aforementioned abnormalities.

Determination of the specific type(s) of asphyxia operative in a particular case, the cause of death, and the manner of death is dependent on information elicited during the medicolegal death investigation—namely, history (circumstances), scene investigation, and postmortem examination (including appropriate ancillary radiographic and laboratory studies).

See also the following:

• Autopsy Request Process

• Adjuncts to the Forensic Autopsy

• Religions and the Autopsy

• Autopsy of the Transplant Recipient

• Autopsy Rate and Physician Attitudes Toward Autopsy

• Universal Precautions and High-Risk Autopsies

• Autopsy Quality Control Metrics

According to the Centers for Disease Control and Prevention (CDC) site's searchable database for Multiple Cause of Death 1999-2004, based on death certificates for United States residents, there are approximately 20,000 accidental and nonaccidental deaths within that period attributable to various types of mechanical asphyxia, such as drowning, hanging, strangulation, and suffocation. ^[1]

The most common causes of asphyxial deaths differ among age groups. Drowning accounts for the overwhelming majority of asphyxial deaths in the 1-4 year age group, whereas hanging, strangulation, and drowning are the most common in the 35-44 year age group (see the image below).

Homicidal asphyxia is relatively uncommon and accounts for less than 5% of homicide cases nationwide, ranking behind firearm injuries, sharp force wounds, and blunt force injuries. ^[2]

Breathing and respiration are complicated processes that have several components. The normal sequence is as follows:

1. Environmental oxygen delivered into the lungs (ventilation)

2. Oxygen diffuses from the air into the blood (pulmonary gas exchange)

3. Blood delivers oxygen to tissues (gas transport)

4. Cells uptake and then utilize oxygen for energy production

Cellular respiration creates carbon dioxide. The carbon dioxide travels in reverse of oxygen and is eliminated from the body via exhaling. Normal breathing entails a patent airway, ability to expand the chest cavity via contraction of intercostal muscles and a functional diaphragm. Defects involving any of the above steps can result in asphyxia.

The brain is the organ most sensitive to hypoxia. Asphyxial deaths typically involve respiratory arrest with bradycardia/asystole because of the hypoxia-induced dysfunction of the respiratory centers in the brainstem. ^{[3, 4]} Individuals with comorbidities such as heart disease can be less tolerant of hypoxia, and relatively minor episodes of hypoxia can exacerbate the preexisting disease and, on occasion, precipitate a lethal cardiac rhythm disturbance. Asphyxia-related acidosis (respiratory and/or metabolic) may also have detrimental consequences.

Tissue hypoxia

Tissue hypoxia can occur for a few basic reasons. First, there may not be enough oxygen content within arterial blood even though the blood flow is normal. This usually occurs when breathing is impaired or when the inhaled air is deficient in oxygen. Second, blood flow and oxygen content are normal; however, the blood does not release oxygen appropriately, or the cells do not utilize it. Chemical asphyxiants such as carbon monoxide (CO) and cyanide (CN) operate in this fashion. Third, the amount of oxygen is normal, but there is restriction of the blood flow to the tissue, hence, lack of oxygen delivery and carbon dioxide pickup for elimination.

Restriction of blood flow

Restriction of blood flow from and to the brain is typically the major feature in nonjudicial hanging or strangulation. There is a significant difference in the amount of force required to occlude the adult airway and cervical blood vessels. Compression of the neck blood vessels is sufficient to cause unconsciousness and death. Thus, unconsciousness and death may occur without significant compromise of the airway.

Table 1. Adult Neck Structures and the Compression Pressures Needed to Cause Unconsciousness and Death (Open Table in a new window)

A medicolegal death investigation is performed to evaluate the cause and manner of a death that occurs suddenly and unexpectedly; that occurs under suspicious circumstances; that may be due to "non-natural" causes such as violence or chemical agents; or, that occurs under other statute or regulation defined circumstances.

Deaths involving asphyxia typically fall within the jurisdiction of the medical examiner or coroner and are evaluated using a systematic medicolegal death investigation—examination of the circumstances, scene, and victim.

Asphyxia is generally categorized as being either mechanical or chemical. There are various entities in each of these categories, and there is overlap among some of the entities. One or more entity can be operative in a particular case.

Chemical vs mechanical asphyxia

Chemical asphyxia involves the reaction between a chemical and tissue/cell that results in the interference of oxygen uptake, release, and/or utilization. Examples of chemical asphyxiants include carbon monoxide (CO), cyanide (CN), and hydrogen sulfide (H₂ S). See the following image.

Mechanical asphyxia involves some physical force or physical abnormality that interferes with the uptake and/or delivery of oxygen. Most mechanical asphyxiants affect breathing or blood flow, the latter usually due to neck vessel or thoracic compression. Breathing an oxygen-deficient atmosphere is typically considered a type of mechanical asphyxia.

There are several subtypes of mechanical asphyxia, which are discussed below.

Suffocation (smothering)

The nose and/or mouth and/or upper pharynx are occluded by an object or body part in such a way that adequate breathing cannot occur. Examples include a pillow or hand over the nose and mouth, a gag, and a head encased by a plastic bag.

Environmental asphyxia

When atmospheric oxygen is insufficient either due to exclusion, depletion, or displacement, environmental asphyxia may occur. This type of asphyxia is often considered a type of suffocation.

Choking

Choking involves the blockage of internal airways (posterior pharynx, larynx, trachea, and/or bronchi) by a foreign object (eg, toy balloon lodged in child's airway, food bolus impacted at epiglottis). See the image below.

Aspiration

Aspiration consists of the inhalation of nonbolus or nondiscrete foreign material (eg, regurgitated stomach contents) or site-inappropriate material. Site-inappropriate material includes such things as inhaled blood secondary to trauma. When aspiration leads to death, the "cause of death" is attributed to the condition (disease or injury) that led to the aspiration.

A special type of aspiration is drowning. Drowning is defined by the 2002 World Congress on Drowning as the process resulting in primary respiratory impairment from submersion/immersion in a liquid. ^[5] The vast majority of drownings are the result of immersion/submersion in water.

Compression (traumatic) asphyxia

Compression or traumatic asphyxia involves the presence of external force on the chest and/or abdomen that prevents expansion of the chest that is necessary for proper breathing (eg, constricting snake, overlying) or causes a rapid increase in intrathoracic pressure with consequent vascular pressure effects (eg, car falling on top of a mechanic). ^{[6, 7]} See the following images.

Postural (positional) asphyxia

Postural or positional asphyxia is caused by the position of the body or part of the body leading to airway restriction, vascular compromise, or breathing fatigue (eg, upside down suspension for prolonged period). Often, there is a degree of physical and/ or mental impairment either due to trauma or intoxication. See the image below.

Strangulation

Application of force to the neck in such a way that the force applied is the result of other than the weight of the victim's body defines strangulation. Strangulation can be "manual" (using hands to compress the neck, also known as throttling), "ligature" (using an object such as a cord, wire, cloth, etc, to constrict the neck), or yoking (using the forearm to apply neck pressure). The proper use of so-called "neck restraint holds" are examples of controlled nonlethal strangulation.

Hanging

Hanging consists of the application of force to the neck in such a way that the force applied is primarily the result of the weight of the victim's body. Contrary to popular belief, there does not have to be full suspension of the body for hanging to cause unconsciousness or death (ie, the body can touch the floor), as shown in the image below.

Hanging is typically subclassified as nonjudicial or judicial. Nonjudicial hanging involves compression of the neck blood vessels with or without significant airway compression. Judicial hanging is designed to fracture and dislocate the upper cervical spine, thereby disrupting the upper cervical spinal cord and/or brainstem.

Autoerotic asphyxia

Autoerotic asphyxia is a purposeful solo activity during which an asphyxia-inducing apparatus or technique is used to enhance sexual stimulation and inadvertently causes death. Nearly all decedents are male. Cross-dressing and/or bondage are common. See the image below.

The scene findings in asphyxial deaths are varied, reflecting the wide range of conditions that can lead to this condition. Law enforcement and medicolegal investigators should be aware that scene findings pointing the asphyxial nature of a death may be subtle in some cases.

Reenactments of pediatric death scenes involving unsafe sleep conditions have been useful in elucidating the causes and manners of death in these cases. Caretakers are usually remarkably honest in showing the position of a child wedged between a bed and wall space, face down in multiple blankets, or in revealing co-sleeping (see the following images). ^[8] (See also Forensic Scene Investigation.)

In cases of autoerotic asphyxia, the victim is frequently in various stages of undress, surrounded by pornographic material and sexual aids. This setup can be embarrassing for the decedent's family or friends, and consequently, they may remove the ligatures/binding, move the body, or otherwise "clean up" the scene before notifying authorities.

Establishing the manner of death relies on accurate documentation of scene findings. Notes suggesting intent ("suicide notes") are useful but not necessarily definitive in establishing suicide, and they must be interpreted in the light of information generated by the history, examination, and/or scene findings. Excessive unpaid bills, overdrawn bank account statements, job firing notices, and eviction letters can be motivation for suicide and should be documented.

Although most motor vehicle crash-related deaths are due to blunt trauma, asphyxia occasionally causes death in this setting. Vega and Adams and Conroy et al reviewed various types of asphyxia in motor vehicle crashes. ^{[9, 10]} Often, the victim's body may be moved during the rescue efforts. It is imperative to determine the initial post crash position of the body and the location of the vehicle in relation to the body (see the following image).

Similarly, successful evaluation of the scene in cases involving a vitiated atmosphere can be difficult due to rescue measures that can include forcing fresh air into the scene of death. Untoward effects experienced by initial rescuers who breathed the "original" air at the death scene can offer critical information about atmospheric conditions experienced by the victim.

Historical information is extremely important in arriving at the correct understanding of a particular death, especially when multiple potential causes of death are present. For example, if a neck compression restraint hold caused death by asphyxia (excluding the scenario of delayed airway occlusion due to neck structure injury), the victim should remain unconscious after the neck hold was released. A history of the victim verbalizing or carrying out volitional activity after the neck pressure was released is not consistent with death being due to the direct effect of the neck compression.

The forensic pathologist is trained to collect and preserve trace evidence. When a ligature is present, the ligature is removed with the knot intact. Even in cases in which ligatures have been removed, traces of foreign material may remain on the skin and can be collected for analysis (see the following image).

In homicidal cases of mechanical asphyxia, the assailant must be relatively close to the victim, and defensive maneuvers may result in transfer of evidence from the assailant to the victim and vice versa. Because mechanical asphyxia, especially strangulation or smothering, is a convenient way to kill in association with sexual activity (usually, but not always, forced), evidence of sexual activity should be sought in an asphyxial death occurring in this scenario. The presence of bite mark evidence should be specifically sought in this type of case. Fingernail clippings/scrapings should be performed to preserve evidence for future analysis.

There are no pathognomonic signs of death by asphyxia. However, there are findings that are characteristically associated with the various forms of asphyxia. The nature and extent of these findings depend on the mechanisms(s) of asphyxia in the particular case, including features of the victim and, in some cases, the assailant. Even the presence of a ligature mark on the neck in a murder is not necessarily indicative of death by ligature strangulation, only that a ligature compressed the neck to some degree. Nevertheless, interpreting the constellation of anatomic findings in conjunction with other investigative information allows most asphyxial deaths to be assessed accurately and reliably.

There are several common findings in asphyxial deaths, which may be present in multiplicity or not at all, such as the following:

• Congestion of the face (plethora) due to venous congestion and poor venous return to the heart (see the image below)

  Congestion of the face and cyanosis.

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• Cyanosis due to excessively deoxygenated hemoglobin in the venous blood (see the image above)

• Facial edema due to increased venous pressure causing tissue fluid transudation (see the image below)

  Facial and upper neck edema.

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• Petechiae in the eyelids, conjunctivae, sclerae, face, and gums due to raised pressure in the microvasculature. These are usually related to arterial blood flow persisting after venous flow is impeded. See the following images.

  Petechiae in the eyelids, sclerae, and face due to ruptures of the microvasculature.

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  Gingival petechiae.

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• Injury to skin and soft tissues of the central face, cheeks, lips, and/or neck.

• Internal neck structure damage due to applied force, particularly to the hyoid bone and laryngeal fractures (see the image below)

  Hyoid bone and laryngeal fractures due to manual strangulation.

  View Media Gallery

• Airway obstruction by tissue (most commonly the tongue), a gag, foreign material bolus, swollen tissue, or aspirated nonbolus material (eg, blood, gastric material)

Note that none of the above findings is specific for asphyxia and can be present in other conditions. For example, patients with congestive heart failure may have a congested face with edema. Resuscitative efforts have been known to cause hemorrhage within the soft tissues of the neck. See the following image.

Layer-by-layer dissection of the anterior neck tissues is typically performed after blood has been allowed to drain from the chest and head. This dissection technique allows demonstration of injuries to the neck soft tissues, hyoid bone, larynx, and blood vessels. See the image below.

Radiographic findings in asphyxial deaths are typically limited to identifying fractures of the hyoid and larynx, cervical spine fractures in hangings (occasionally seen in nonjudicial hanging scenarios involving victims who jump from high structures, especially if the victims are elderly or have preexisting cervical spine diseases [eg, osteoporosis, ankylosing spondylitis, osteoarthritis]), or identifying a foreign object in the airway.

Hypoxic/ischemic damage to tissues may be evident if the survival interval is prolonged. The presence/absence of an inflammatory infiltrate (repair process) associated with injuries may allow some assessment of when the injuries were sustained in relation to the time of death.

 

Photography at the scene and in the morgue suite plays an important role in helping to determine and document the findings upon which the cause and manner of death opinions are based. In addition to routine identification and injury photographs, the forensic pathologist's report and/or file should include photographs and written description addressing the following:

• Presence/absence of injuries on the face, oral cavity, neck, chest, abdomen, and extremities (eg, evidence of bondage or restraint)

• All ligatures or bondage/ binding devices before and after removal, if applicable

• Complete description of the ligature (including composition, size)

• Nature of the knot

• Hemorrhage (including the extent and distribution)

• Internal neck or chest injuries and status (structural integrity and degree of pliability) of the hyoid bone and larynx

• Material or object in the airway

Documentation should address specific issues pertinent to the particular case details.

Comprehensive death investigation should include a thorough history, death scene investigation, and appropriate postmortem examination that includes toxicologic, other pertinent laboratory studies (such as carboxyhemoglobin saturation in suspected carbon monoxide poisoning), and appropriate radiologic studies.

Toxicologic findings are often key in helping to understand why someone died. If an individual is under the influence of either legal or illegal intoxicant(s), it may enhance the likelihood of getting into a compromising situation or decrease the likelihood of extrication from a jeopardizing situation (eg, inability to fight off an attacker in strangulation, escape from trapped position that compromises breathing/respiration, or making sound judgment decisions).

See also the following:

• Postmortem Changes

• Postmortem Radiology and Imaging

• Postmortem Vitreous Analyses

• Forensic Toxicology - Drugs and Chemicals

• Forensic Pathology of Thermal Injuries

Several issues may arise during law enforcement investigation and/or adjudication of potential homicidal asphyxial deaths and are briefly discussed below.

Handedness

Determining handedness of the assailant cannot be reliably established. Most adults can strangle with either the dominant or nondominant hand. Specifics of strangulation are also difficult to establish, as it can be accomplished using forehand or backhand, overhand or underhand, 1 or 2 hands.

Absence/presence of neck markings

Fingernail marks on the neck indicate injury to the neck caused by someone with nails sufficiently long to cause marks. The marks may be made by the assailant during strangulation or while attempting to control the victim. Occasionally, marks on the neck are made by the victim during attempts to alleviate pressure on his/her own neck (eg, attempting to remove a ligature). Some ligature marks may have a sufficient pattern to allow recognition of the features of the ligature (eg, woven cord). Determining the nature of a ligature is difficult when a ligature mark is inconspicuous or, sometimes, even when it is prominent. The presence of petechiae are not specific for mechanical asphyxia, and other causes need to be excluded—for example, postmortem extravasation, effects of other problems such as a blood vessel disorder or blood clotting problem.

Some homicidal asphyxial deaths, including suffocation and strangulation, can occur in the absence of demonstrable injuries. The determination of cause and manner of death in such cases can be very problematic and may come down to considering and judging the reliability of witness accounts and/or observations and/or a perpetrator confession.

Time to unconsciousness/death

The time it takes to reach unconsciousness and the time it takes to die of asphyxia are influenced by the nature of the asphyxiant, duration of its application, efficiency of its application, and victim susceptibility. Experimental studies and witnessed (sometimes videotaped) events of neck compression (hanging and strangulation) indicate very rapid loss of consciousness after carotid artery compression. Studies of videotaped nonjudicial hangings have elucidated stereotypical behavior exhibited by the victim following the loss of consciousness. ^{[12, 13]}

The minimal duration of neck compression after loss of consciousness to cause death has not been clearly defined .  All the subjects studied by Rossen and Kabat who were subjected to 100 seconds of total carotid artery occlusion survived. ^[14] DiMaio and DiMaio cited information pertinent to the temporal sequence of events in infant smothering. ^[15] They indicated that during infant smothering there is bradycardia (onset 30 sec after initiation of smothering); decrease in breathing, agonal gasps, then apnea; and, slowing and flattening of the electroencephalogram (flattening at 90 seconds). DiMaio and DiMaio reported that the infant will not usually auto-resuscitate once there is apnea.

Mechanical asphyxiation and deaths in custody

The death of a suspect temporally related to apprehension by law enforcement can be consequent to a variety of potential causes and mechanisms. Occasionally, there may be an issue as to whether or not action by law enforcement personnel caused or contributed to death. Some of these actions potentially involve asphyxia.

In some cases, the intention is to produce nonlethal mechanical asphyxia (eg, application of neck restraint hold), whereas in others mechanical asphyxia is inadvertent (eg, thoracoabdominal compression during a "dog pile"). In other cases, issues as to whether or not a particular restraint technique caused or contributed to asphyxia may need to be addressed. Examples of these issues include the effects of the restraint position (eg, restrained in the prone position with or without hogtieing) and the effect of chemical control agents (eg, tear gas, mace, pepper spray).

Neck restraint holds

Neck restraint holds, most typically involving carotid compression, have been used fairly commonly and represent a form of controlled strangulation. The hold is applied until unconsciousness ensues; the subject is then immediately cuffed, and the hold released before the onset of any irreversible cerebral ischemic damage. Rarely, the delayed onset of asphyxia, sometimes lethal, may result from unrecognized laryngeal damage sustained during an episode of neck compression.

Prone restraint positions

For a period of time, restraint position was often implicated as being causal or contributory to death. This most often involved persons who had been hogtied and left in the prone position. Implication of the prone hogtied position was primarily based on studies in which recovery of oxygen saturation (as measured by a transcutaneous earlobe blood oxygen saturation probe) following exercise took longer in hogtied volunteers than in those who were not hogtied. ^[16] However, subsequent studies using more accurate measuring techniques (arterial blood gas measurements) failed to confirm the previous studies. ^[17] Currently, the prone restraint position (with or without hogtie) is generally considered a neutral position.

Thoracoabdominal compression

Inadvertent development of asphyxia consequent to thoracoabdominal compression sustained during apprehension may be an issue. Pressure can be applied to the chest, most commonly to the back, to facilitate the application of manacles. In many cases, the pressure is applied to the shoulders and lower back, buttock, or upper thighs using less than the full body weight of the restraining personnel. In other cases, multiple persons attempting to gain control of an unruly suspect can apply less targeted and less controlled pressure.

Although it is clear that thoracoabdominal compression can cause death if it is heavy enough and prolonged enough, the quantity and duration of thoracoabdominal pressure necessary to cause or contribute to death is less clear.

No significant differences in oxygen saturation or end tidal carbon dioxide were demonstrated in human volunteers between sitting, maximal restraint position or maximal restraint with up to 50 pounds (lb) of weight on the back. ^[18] Other studies indicate that 225 lb of pressure uniformly distributed over the back reduces the minute ventilation volume (MVV) to about 60% of predicted. ^[19] Thus, the targeted, relatively brief application of pressure to the back during cuffing (eg, knee on the back with less than full body weight applied) is not likely to cause significant, if any, asphyxia. However, the authors are of the opinion that the prolonged continuous application (probably measured in minutes) of extreme pressure on the chest (such as the nearly full body weight of several officers) is capable of causing death.

Summary

To appropriately address these issues, as in any death investigation, detailed descriptions of the decedent and others involved in the incident are essential. A second-by-second account of the incident including the locations, actions, and effects of the actions of each of the participants is critical to properly evaluating the incident. Evidence of consciousness and volitional activity of the decedent following the release of any restraint hold or removal of weight from the chest is important to ascertain. Excluding delayed asphyxia caused by a structural internal injury (eg, laryngeal fracture), the immediate effects of a neck restraint hold or pressure applied to the chest did not result in death if the decedent regained consciousness, as evidenced by demonstrating awareness of his surroundings, intelligible vocalization, and/or volitional activity.

The reader is directed to the following sources for more information:

• Prahlow JA, ed. Basic Competencies in Forensic Pathology: A Forensic Pathology Primer. Northfield, Ill: College of American Pathologists; 2006.

• Dolinak D, Matshes EW, Lew EO. Forensic Pathology: Principles and Practice. Amsterdam, The Netherlands: Academic Press; 2005.

• DiMaio VJ, DiMaio D. Forensic Pathology. 2^nd ed. Boca Raton, Fla: CRC Press; 2001:234.

• Froede RC, ed. Handbook of Forensic Pathology. 2^nd ed. Boca Raton, Fla: CRC Press; 2003.

• Graham MA, Hanzlick, R. Forensic Pathology in Criminal Cases. 2^nd ed. Carlsbad, Calif: Lexis Law Publishing; 1997

• Spitz WU, Spitz DJ, Fisher RS, eds. Spitz and Fisher's Medicolegal Investigation of Death: Guidelines for the Application of Pathology to Crime Investigation. 4^th ed. Springfield, Ill: Charles C. Thomas; 2006.