Veterinary Forensic Pathology, Volume 2

© Springer International Publishing AG 2018

Jason W. Brooks (ed.)Veterinary Forensic Pathology, Volume 2https://doi.org/10.1007/978-3-319-67175-8_1

1. Drowning and Bodies Recovered from Water

Beverly J. McEwen¹   and Jodie A. Gerdin²  

(1)

Animal Health Laboratory, Ontario Veterinary College, University of Guelph, 419 Gordon Street, Building 89, Guelph, ON, Canada, N1G 2W1

(2)

Antech Diagnostics, 9 Schilling Road, Suite 211, Hunt Valley, MD 21031, USA

Beverly J. McEwen (Corresponding author)

Email: bmcewen@uoguelph.ca

Jodie A. Gerdin

Email: Jodie.gerdin@antechmail.com

1.1 Introduction

1.2 The Process and Mechanism of Drowning

1.2.1 Autonomic Conflict: The Diving Response and Cold Shock Responses in Cold Water Immersion

1.3 Morbidity

1.4 Macroscopic and Microscopic Lesions of Drowning

1.5 Postmortem Changes

1.6 Case Report of Drowning []

1.7 Ancillary Tests and Methods Used in Determination of Drowning

1.7.1 Lung Weights

1.7.2 Diatoms

1.7.3 Electrolyte Tests

1.8 Summary

References

1.1 Introduction

Determining the cause of death in animals recovered from bodies of water, swimming pools, or other water-containing vessels is challenging. The key question is Was the animal alive when it entered the water? [1]. Animals recovered from water may had drowned, died from other causes in water, died on land, and either have fallen into water or have been disposed of in water (Fig. 1.1). Animals that have drowned may be translocated to other sites, including land, by tides, currents, people, or other animals (Fig. 1.1). Postmortem changes due to submersion, injuries, or scavengers introduce artifacts and obscure lesions. The diagnosis of drowning in animals and people is usually one of exclusion, requiring information from the crime scene, recovery scene, the medical history, or reliable witness accounts [2–5].

Fig. 1.1

Possible scenarios of bodies recovered from water

The definition and terminology associated with drowning, as with other types of asphyxia, are varied [6, 7]. Submersion signifies that the entire body is under water, whereas immersion refers to the body being partly covered with water, although the airway must be immersed for drowning to occur [8]. Terminology prior to 2002 was confusing: near-drowning was used if the person survived even temporarily and drowning if it was fatal; both were then divided into those cases in which aspiration of water was present or absent [7]. The following adjectives describing drowning outcomes are no longer recommended: passive, silent, wet, dry, active, secondary drowning [7, 8] or near-drowning [9]. In 2002, the definitions of drowning and its possible outcomes were decided by an international group of experts: Drowning is the process of experiencing respiratory impairment from submersion/immersion in liquid with outcomes of death, morbidity or no morbidity [7]. The revised terminology is used in at least one review of canine drowning [10], and we recommend that it be adopted by veterinarians [11].

An estimated 388,000 people drown annually, and it is the third leading cause of accidental death worldwide [12]. The frequency of drowning in animals is unknown, although a website that tracks animal abuse (pet-abuse.​com) listed 205 drowning cases out of 19,464 cases (1.05%) in its database (October 20, 2016). The accuracy of this statistic is not known as there is no mandatory reporting of animal drowning or cruelty in most jurisdictions, although databases such as the newly implemented National Incident-Based Reporting System at the Federal Bureau of Investigation should provide improved estimates [13].

The peer-reviewed veterinary literature on accidental and non-accidental drowning in animals is scarce [1, 10, 14–17], although the topic is covered briefly in several veterinary forensic textbooks [18–20]. Reports of accidental drowning in animals include situations involving electrical shock, entrapment, entanglement, or victims with pre-existent medical conditions such as ataxia and epilepsy [14, 21]. Experiments in which dogs or other animals were drowned to determine physiological and biochemical responses to various volumes, temperatures, and salinity of water or other liquids provide information into the drowning process [22–35]. The lack of consideration for the welfare of animals used in these experiments, performed between 20–200 years ago, is disturbing. We recognize, however, useful information can be gained from these experiments and applied to veterinary forensic pathology for the benefit of animals today [1, 11]. The objective of this paper is to review the mechanisms, lesions, and diagnostic issues associated with drowning in nonaquatic companion animals.

1.2 The Process and Mechanism of Drowning

The central mechanism of drowning is rapid and persistent hypoxemia following the introduction of liquid at the entrance of the airway [23, 25, 34, 36–38]. The drowning process (Fig. 1.2), reviewed extensively in the medical literature [2, 3, 5, 7, 8, 36, 37, 39, 40], is largely based on experiments in dogs and incorporates behavioral and biological responses to drowning [23, 29, 30, 34, 38, 41]. This has been categorized into the five phases of drowning (Fig. 1.3) [42].

Fig. 1.2

The drowning process

Fig. 1.3

The five phases of drowning

The drowning process is complex, involving sequential and overlapping cardiorespiratory reflexes, electrolyte and blood gas abnormalities, aspiration and swallowing of liquid, vomition, struggling, involuntary movements, physical exhaustion, and breathlessness or air hunger [43] eventually culminating in death [44] (Fig. 1.2). Survival time is inversely proportional to the volume of water rather than the temperature or salinity [23, 38].

Upon immersion, there may be a few deep respirations, although breath holding and vagal-mediated laryngospasm usually occur upon submersion [26, 41] and arterial oxygen decreases abruptly. As little as 2 mL of water contacting the larynx or aspirated into the lung causes laryngospasm in dogs, and aspiration of only 5 mL of salt- or freshwater in dogs causes rapid and persistent hypoxia without significant hypercarbia [23, 30, 38]. Laryngospasm may last 1.5–2 min during which arterial CO2 increases [25] and acidosis develops [21, 34, 36]. Bradycardia [23, 30, 45] occurs immediately following submersion [26, 33] or after brief tachycardia [32, 34]. Blood pressure immediately increases and then progressively decreases [23, 32].

Submerged, non-anesthetized dogs struggle violently for 1.5 min [41, 42]. Thoracic inspiratory movements caused liquid to be swallowed, but because the glottis is closed [9, 30, 45], ventilation and gas exchange does not occur. Aspiration will occur with continued submersion whether the animal is conscious or not; if unconsciousness occurs due to hypoxemia, the larynx relaxes and water is aspirated [46]. If the animal is conscious, water is aspirated and swallowed due to deep inspiratory gasping that lasts up to 3.5 minutes [41, 47]. After 3 minutes, spasmodic convulsions and seizures occur [32, 41], and overdistension of the stomach with water causes violent vomition [41]. Electroencephalograph (EEG) activity varies with the duration of initial apnea [45]: cardiac asystole or observed death occurs usually within 5 min but occasionally up to 10 min following submersion [25, 26, 32, 38, 41, 42, 47]. The initial hypoxemia in fresh- and saltwater drowning is intensified by pulmonary edema and is exacerbated by exponential catecholamine release, subsequent vasoconstriction, cardiac arrhythmias [34], pulmonary hypertension, and right to left intrapulmonary shunting [34, 37, 48].

Electrolyte and intravascular volumetric changes in drowning depend on the salinity and/or volume of water aspirated. The biochemical effect of water salinity is primarily osmotic [23, 24, 28, 29] and not temperature related [34]. Distinguishing between saltwater and freshwater drowning is given little clinical significance in people [9, 37], although some think that it does impact the likelihood of successful resuscitation and survival [34]. The location of drowning, however, is critical to the forensic investigation [49].

In dogs, aspirated freshwater enters the circulation within 3 minutes [23, 46], and an estimated 10% of the body weight can be absorbed by the lungs during freshwater immersion [34]. The changes are transient due to redistribution of fluids within the body [23, 25], and dilutional hyponatremia was not present in a case series of dogs and cats resuscitated following submersion in freshwater. However, hemodilution and electrolyte alterations may persist if the volume of water aspirated is 22 mL/kg or greater [25, 28]. Volume-dependent ventricular fibrillation is common, occurring in many, but not all dogs drowned by 9.1 mL/kg but not by 4.5 mL/kg [23]. The ionic charges responsible for the surface-tension properties of surfactant are altered by freshwater which results in alveolar instability and pulmonary atelectasis [23, 40]. Atelectatic alveoli are perfused but not ventilated, resulting in right to left intrapulmonary shunting [40], further exacerbating the hypoxemia.

Death due to saltwater aspiration requires half the aspirated volume as for freshwater (Table 1.1) [23, 26, 34, 38, 50, 51]. The aspirated hypertonic water pulls fluid from the circulation into the alveoli, leading to the damage of the basement membrane, washout of surfactant, and reduced lung compliance [52]. Ensuing pulmonary edema decreases the ventilation-to-perfusion ratio, and right to left intrapulmonary shunts develop [37]. Type I and II pneumocytes [53–55] and alveolar-capillary endothelium [50, 53] are damaged by both fresh- and saltwater. Neither hemolysis nor ventricular fibrillation are features of experimental seawater drowning [28, 29].

Table 1.1

Volumetric and electrolyte changes in saltwater compared to freshwater drowning [24–26, 28, 34, 38, 50, 51]

Drowning ultimately results in progressive cerebral hypoxia [37] and death. In people, irreversible injury occurs in the selective regions of the brain within 4–10 min, and persistent coma develops within a few minutes after that time period [56, 57]. The precise outcome of hypoxic injury due to drowning is difficult to predict even if the individual is resuscitated [58].

1.2.1 Autonomic Conflict: The Diving Response and Cold Shock Responses in Cold Water Immersion

People suddenly submersed in water 5 °C below body temperature may become unconscious and develop cardiac arrhythmia, possibly due to vagal stimulation and/or catecholamine release [9, 34, 59–62]. The parasympathetic and sympathetic responses following rapid submersion and breath holding are the diving response and cold shock response, respectively [61]. These responses are often discussed as isolated physiologic reflexes but in reality are concurrent reflex reactions that produce a predictable, often opposing complement of physiological events (Table 1.2) [62, 63]. The diving response is postulated to be protective if the animal is suddenly immersed in water by inhibiting respiration and producing bradycardia; however, it is frequently exacerbated by anxiety and/or antagonized by the cold shock response.

Table 1.2

Diving and cold shock responses [4, 60–65]

The diving reflex response of apnea and bradycardia, presumed present in all vertebrates [61, 62], is activated by the receptors of the face via the ophthalmic and maxillary divisions of the trigeminal nerve, which cause reflex inhibition of the medullary respiratory center [4]. Vagal receptors in the pharynx and larynx produce similar responses [61]. The response is enhanced as the water temperature decreases [4]. Cold thermoreceptors of the skin mediate the sympathetic-associated cold shock response which causes tachycardia, hyperventilation, peripheral vasoconstriction, and hypertension [60, 61]. Both responses can cause cardiac arrhythmias independently or together by issuing conflicting, simultaneous signals to the heart [61, 63, 66–68].

Within 2 min of submersion in cold water, core body temperature decreases more rapidly and deeply than with immersion [34], due to the aspiration of larger quantities of water and contact with the large surface area of the pulmonary circulation. Primary hypothermia due to submersion causing rectal temperatures to drop to 20 °C or below [69] is fatal. The onset and duration of cardiorespiratory and cerebral responses were similar in dogs which were submerged in 0–1 °C and had their tracheas clamped [47] to those submerged in normothermic or cold water but allowed to aspirate water [28–30, 41]. The absolute and relative decreases in rectal and cerebral temperatures were proportional to the submersion time.

1.3 Morbidity

A case series of 25 dogs and 3 cats resuscitated following submersion in freshwater concluded that the prognosis for survival is good if respiratory tract failure and cardiac arrhythmias do not develop [21]. Level of consciousness upon presentation, even coma, was not associated with outcome [21]. Complications in animals that survive drowning include reduced mentation or neurological deficits [50], non-cardiogenic pulmonary edema [70], septic pneumonia [15], and acute respiratory distress syndrome [21].

1.4 Macroscopic and Microscopic Lesions of Drowning

Tables 1.3 and 1.4 list macroscopic and microscopic lesions in drowned animals. In individual cases, these lesions may or may not be present. Emphysema aquosum, a term used in medical forensic pathology describing overinflated, waterlogged lungs and alveolar dilation, thinning of alveolar septa, and compression of alveolar capillaries histologically [4, 71], should be avoided in veterinary pathology. Instead, lesions should be appropriately and fully described for clarity. The presence, severity, and type of pulmonary macroscopic and microscopic lesions are frequently not uniform and often vary within a single histological section (Figs. 1.4 and 1.5).

Table 1.3

Macroscopic lesions of drowning documented in animals [1, 11, 17, 18, 33, 39, 71, 73–75]

Table 1.4

Microscopic lesions of drowning documented in animals [11, 18]

Fig. 1.4

Lung, canine, aspirated foreign material in drowning. Abundant foreign material is present in an airway (Courtesy of Dr. M. Hazlett)

Fig. 1.5

Lung, canine. Same lung as in Fig. 1.4, adjacent to area with foreign body demonstrating only mild congestion and hemorrhage (Courtesy of Dr. M. Hazlett)

In cases of suspected drowning, the appearance of the fur should be recorded as wet or dry or if the hair is dried in clumps or spikes, indicating recent wetness. Distended, heavy, edematous lungs that fail to collapse and stable froth in the upper airway including the mouth and nasal passages are characteristic of drowning (Fig. 1.6) but not specific, as these may be due to other causes [37, 71].

Fig. 1.6

Lung, canine, drowning. The lungs are distended, edematous with emphysema, petechiae, random atelectatic foci, and subpleural hemorrhages (Courtesy of Dr. S. McDonough)

A small to moderate amount of watery, colorless to pale pink-brown tracheal foam is a fairly common postmortem artifact in a variety of species, especially in the setting of barbiturate euthanasia, and may be especially prominent in horses [72]. Stable froth in the tracheobronchial tree (Fig. 1.7), larynx, and nostrils can only be produced by a live animal [18] and may also arise with other causes of pulmonary edema [37]. Blood-tinged froth is produced by hemolysis of red blood cells within the edema fluid [42]. A mare that initially survived drowning had stable red froth at the nares and continued to expectorate this material by paroxysmal coughing for a few hours after treatment was initiated [14]. Macroscopic or microscopic foreign material deep within the tracheobronchial tree and lungs is compatible with aspiration (Fig. 1.4) [18]. In people, the external foam and stable airway froth may persist for several days, even with the onset of putrefaction [37]. Both features may disappear or be altered by the effects of time, handling, storage, and freezing of the body prior to the postmortem examination [11]. This is another reason why investigators should provide, and pathologists should request, photographs and documentation of the animal at the recovery scene.

Fig. 1.7

Trachea, canine, drowning. Abundant stable froth and red-tinged fluid are present in the trachea (Courtesy of Dr. S. McDonough)

The amount of liquid penetrating the lungs depends upon the respiratory efforts, laryngospasm, and time of cardiac arrest [46]. Most people die with typical pulmonary lesions of marked edema and abundant tracheal froth (wet drowning), whereas 2–15% is classified as drowning without discernible evidence of aspiration (dry drowning) [46]. Dry lungs in human victims attributed to sudden cardiac arrhythmias including channelopathies [61, 76], cardiac arrest, or laryngospasm following submersion [46]. Dry drowning may represent not only one end of the spectrum of drowning lesions but also deaths in water due to natural causes and bodies that were disposed of in water [9, 42, 46]. The significance and pathophysiology of dry drowning is debated in medical forensic pathology [46], and as stated previously, this term should be avoided. In dogs, even low volumes of aspirated water caused hypoxemia and decreased lung compliance [24, 38]. Lungs lacking evidence of aspiration are documented in experimental drownings of muskrat and beavers that had a mucus plug in the trachea [33]. In dogs, lack of significant fluid aspiration was attributed to laryngospasm [41] or the failure to gasp [30] although the latter seems unlikely.

Pleural effusion, subdural discoloration of the petrous temporal bone due to congestion, or hemorrhage in the mastoid process and middle ear, hemorrhage in the neck muscles, a contracted spleen [3, 4, 37], subpleural intra-alveolar hemorrhages with blurred margins (Paltauf’s or Rasskazov-Lukomskij spots) [77], and hemolytic red staining of the aortic intima [78, 79] and left heart [80] are additional findings in people that may support a diagnosis of drowning. Subpleural hemorrhages were present in lungs from a drowned dog (Fig. 1.6).

Weights such as blocks, tires, or chains bound to the animal indicate intentional submersion of the body but do not indicate if the animal was alive or dead at the time of submersion [11]. Lesions of blunt force trauma of the head, neck, or limbs may be present in animals that were forcibly immersed or submerged in water [18, 20, 81].

The appearance and approximate volume of gastric contents should be documented, as swallowing water is common during drowning [11, 30, 41]. Gastric mucosal lacerations due to overdistension of the stomach with water are sporadically reported in human drowning victims [37]. Elevated liver enzymes in animals resuscitated following submersion were attributed to hepatic hypoxia and necrosis, but this cannot be confirmed as histopathological examination of the liver has not been described [21] Hepatocellular necrosis was confirmed in one dog that aspirated water from a drainage ditch, but it cannot be determined if this was due to the initial drowning or sequelae such as heart failure [15]. Myocardial lesions of contraction bands and rupture of intercalated discs in the cardiac myocytes of rats drowned in either salt- or freshwater may be due to excessive catecholamine release [82].

A thorough postmortem examination will aid in determining if significant intercurrent diseases are present [21], and a medical history of conditions such as epilepsy will also be useful particularly in determining why an animal was unable to extricate itself from the drowning medium [11, 18]. Hyponatremic encephalopathy due to excessive intake of freshwater (water intoxication) should also be considered as a contributing or alternative cause of death, particularly in animals that play or train in freshwater [83].

1.5 Postmortem Changes

The postmortem submersion interval (PMSI) and postmortem changes that occur while in water and following retrieval may make examination and determination of the cause of death even more challenging [11]. Early changes are skin maceration, lividity, rigor mortis, and algor mortis, and late changes include initial putrefaction, advanced putrefaction including adipocere formation, and skeletonization [37, 84]. Adipocere is a waxy material on bodies submersed in water produced by degradation of adipose tissue by endogenous and bacterial enzymes [85]. Postmortem changes in the water, as on land, are time and temperature dependent [37]. The lower temperatures of bodies of water usually retard rigor mortis and accelerate body cooling [37, 84]. Decomposition while in water is slower than on land; however, once a body is removed from the water, it rapidly accelerates. The body initially sinks and then rises to the surface once putrefactive gases increase buoyancy [85]. If the water