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Review Article *Corresponding author Bhagya Sannananja, Department of , University of Washington, 1959, NE Pacific St, Seattle, WA Near-: Epidemiology, 98195, USA, Tel: 830-499-1446; Email: Submitted: 23 May 2017 Pathophysiology and Imaging Accepted: 19 June 2017 Published: 22 June 2017 Copyright Findings © 2017 Sannananja et al. Carlos S. Restrepo1, Carolina Ortiz2, Achint K. Singh1, and ISSN: 2573-1246 3 Bhagya Sannananja * OPEN ACCESS 1Department of Radiology, University of Texas Health Science Center at San Antonio, USA Keywords 2Department of Internal Medicine, University of Texas Health Science Center at San • Near-drowning Antonio, USA • Immersion 3Department of Radiology, University of Washington, USA\ • Imaging findings • / • Magnetic resonance imaging Abstract • Although occasionally preventable, drowning is a major cause of accidental death • X-Ray computed worldwide, with the highest rates among children. A new definition by WHO classifies • Nonfatal drowning drowning as the process of experiencing respiratory impairment from submersion/ immersion in , which can lead to fatal or nonfatal drowning. Hypoxemia seems to be the most severe pathophysiologic consequence of nonfatal drowning. Victims may sustain severe organ damage, mainly to the brain. It is difficult to predict an accurate neurological prognosis from the initial clinical presentation, laboratory and radiological examinations. Imaging plays an important role in the diagnosis and management of near-drowning victims. Chest radiograph is commonly obtained as the first imaging modality, which usually shows perihilar bilateral pulmonary opacities; yet 20% to 30% of near-drowning patients may have normal initial chest radiographs. Brain manifest on CT by diffuse loss of gray-white matter differentiation, and on MRI diffusion weighted sequence with high signal in the injured regions. This review presents the epidemiology and pathophysiology of nonfatal drowning and a detail description of the most common multisystem imaging findings.

INTRODUCTION accounting for 0.7% of deaths worldwide [1]. CDC analyses from National Vital Statistics System and National Electronic Injury Worldwide, some half a million people die each year from Surveillance System for 2005-2009, indicated that each year an drowning, and for each death, there are one to four drowning average of 3,880 persons were victims of fatal drowning and 34% incidents serious enough to warrant hospitalization [1]. Organs of all fatalities were persons under 20 years old and almost four such as the brain, and kidneys are mainly affected by times more common in males. During the same period, there were drowning accidents. However, the greatest permanent harm on average 5,789 persons treated annually in U.S. emergency in drowning accidents is to the brain, which has negligible departments (ED) for nonfatal drowning cases, which included metabolic substrate reserves to subsist upon in the absence of continuous delivery of oxygenated . Much of the literature “drowning/near-drowning,” and a diagnosis of “submersion”. on near-drowning has concentrated on the respiratory effects Childrenthose classified under 4as years having old a accounted precipitated for or52.8% immediate of the ED cause visits, of of aspiration and on the management of both early and late and children aged 5–14 years accounted for 17.5%. Among respiratory complications such as aspiration and nonfatal incidents occurred in swimming pools. Drowning in have been reported [2-4], but there is limited description of extra naturalchildren water aged settings ≤4 years, increases 50.1% ofwith fatal increasing incidents age and group 64.6% [5]. of thoracicadult respiratory imaging manifestations distress syndrome. seen inThoracic affected imaging individuals. findings The the different imaging techniques in the evaluation of the victim with terms like dry drowning and near-drowning, the WHO ofaim nonfatal of this drowning.article is to review the imaging findings and role of Given the variety and inconsistency of definitions, particularly of experiencing respiratory impairment from submersion/ EPIDEMIOLOGY established in 2002 a new definition of drowning as, “the process Drowning is a leading cause of unintentional injury death, respiratory impairment as the person’s airway goes below the immersion in liquid”[6]. The drowning process begins with

Cite this article: Restrepo CS, Ortiz C, Singh AK, Sannananja B (2017) Near-Drowning: Epidemiology, Pathophysiology and Imaging Findings. J Trauma Care 3(3): 1026. Sannananja et al. (2017) Email:

Central Bringing Excellence in Open Access surface of the liquid (submersion) or water splashes over the face (immersion). If the person is rescued at any time, the process of drowning is interrupted, which is termed a nonfatal drowning. If andinvolvement alveolar opacitiesthroughout throughout the lung bilateral the bilateral fields lungs. [4,20]. These The mosttend the person dies at any time because of drowning, this is termed tocommon coalesce radiographic in the perihilar finding and is thatmedial of diffuse, lung zones hazy ground-glasswith sparing a fatal drowning. Any submersion or immersion incident without of the most lateral portions of the lung including the bases and evidence of respiratory impairment should be considered a water the apices (Figure 1a). The distribution tends to be bilateral, rescue and not a drowning [7]. but may also be asymmetrical with more extensive involvement of the right or left lung (Figure 1b). This imaging presentation PATHOPHYSIOLOGY is macro and microscopically indistinguishable from that of The process of drowning begins with the airway under water, , with alveolar hemorrhage, interstitial edema leading to breath-holding; soon the person can no longer keep and dilation of alveolar spaces found on histopathological his or her airway clear, water entering the mouth is voluntarily examination [21,22]. Air bronchogram is appreciated in those spat out or swallowed. When the inspiratory drive is too high to with denser air-space disease. In the more severe cases, resist, some amount of water is aspirated into the airways, and consolidation may extend to the entire parenchyma of both lungs, with little or no areas of sparing. Parenchymal opacities tend to occurs, but in such cases, it is rapidly terminated by the onset of worsen in the initial 24 to 48 hours before starting to resolve braincoughing hypoxia. occurs as a reflex response. Sometimes (Figure 1c and 1d). In most cases there is complete clearing of As hypoxia, and acidosis ensue, the victim losses week may represent superimposed bacterial pneumonia or adult respiratorythe lungs between distress 3-5 syndrome days. Persistent [23].Diffuse infiltrates areas after of the ground- first lungs, worsening respiratory and metabolic acidosis. The initial glass attenuation characterize high resolution CT, which may cardiovascularconsciousness. response This leads to the to process larger of drowning aspiration is tachycardia into the and , though the worsening hypoxia and acidosis crazy-paving appearance (Figure 2). Nodular and patchy areas of leads to bradycardia, and decreased denserbe associated air-space with consolidation interlobular can septal also be thickening appreciated, configuring randomly a distributed but predominantly in a central distribution [24]. In a multidetector CT study of 28 drowned subjects, Levy et al., fromcardiac submersion output. Atrial of the fibrillation victim to cardiacand other arrest cardiac usually arrhythmias occurs in reported ground-glass opacities with septal lines (89%), with secondsmay occur, to few progressing minutes, although finally to in a very systole unusual [8-11]. cases The reported process in ice water, this process can last up to one hour [12,13]. Hypoxia appears to be the single most important abnormality in death resultant from submersion in water, while acidosis and hypercarbia may contribute secondarily [11,13,14]. Hypoxemia is injury develops secondary to the effects of dysfunction andinitially washout, due to increased apnea but once fluid permeability, aspiration occurs, alveolar acute collapse, lung , ventilation- mismatch and intrapulmonary shunting [7,11,15-17]. A) B) The greatest permanent harm in submersion accidents is to the brain. The brain is sensitive to the timing, duration, and intensity of hypoxia. Irreversible injury develops in the hippocampus, basal ganglia, and cerebral cortex within 4–10 min. Resuscitation at this stage may manifest in memory, movement, and coordination disorders. Only a few additional minutes of hypoxia may result in persistent coma or death [17-19] (Table 1). IMAGING FINDINGS

Chest C) D) Initial imaging evaluation of near-drowning victims is Figure 1 Chest radiographs of three different patients with non-fatal typically performed with conventional chest radiograph. The drowning. Figure 1a: 25-year-old female with non-fatal drowning chest radiograph remains a rapid, simple and cost-effective episode (swamp water). Bilateral airspace disease and consolidation method of initial evaluation of these patients. From the is noted, denser in the central and parahilar regions. Figure 1b: earliest reports on this subject the similarity between imaging 4-year-old female with non-fatal drowning (swimming pool). AP view manifestations of near drowning and pulmonary edema have of the chest demonstrates diffuse bilateral parenchymal opacities in been recognized. The classic papers by Rosenbaum et al and later by Hunter et al., identify three basic imaging patterns: a) normal radiographthe bilateral shows lungs, more ground-glass confluent opacities in the right in the side. bilateral Figure 1c lungs. and radiograph with no obvious abnormality, b) perihilar pulmonary Follow-upFigure 1d: radiograph 26-year-old 24 male hours with later non-fatal shows drowning. progressive Initial bilateral chest edema, and c) generalized pulmonary edema with more diffuse airspace consolidation.

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Drowning

Aspiration

Hypoxia, hypercapnia, acidosis

Acute lung injury Arrhythmia and cardiac failure Acute tubular necrosis

Multi-organ failure

Chest Abdomen Brain Paranasal sinus Spine

Pulmonary edema Fluid and/or sand Cortical edema Air-fluid level Fractures in bowel Consolidation Watershed infarcts Fluid in Periportal edema Reversal sign tracheobronchial tree Periportal edema White cerebellum sand bronchogram

Takotsubo

Table 1

Pathophysiology and imaging findings of near drowning. a predominant apical and parahilar distribution and severe dense consolidation in one third of cases [25]. Pneumothorax, in as much as 50% contained high attenuation sediment. This pneumomediastinum and pneumopericardium are additional highsubjects, attenuation central airwaysediment fluid may was also highly affect prevalent second order (93%) bronchi which [25].Sand aspiration during drowning and near drowning may interstitial pulmonary emphysema and pneumomediastinum findings seen in some patients (Figure 3). Kim et al., detected CT as radiodense material within the affected bronchi (“sand observed bilateral pneumothoraces in 1 of10 near-drowned occur; which can be identified on chest radiograph and chest on thin-section CT in 2 of 6 patients, while Wunderlich et al., Between 20% and 30% of near-drowning patients may have reported in 10% of drowned subjects, but are less common in bronchogram”) [3,26]. normal initial chest radiographs [2,27]. This generally represents near-drowningchildren [2,24,26]. patients Small [25]. bilateral pleural effusions have been less severe cases, with good prognosis, but this is not always the Fluid from different types of aspirated content is commonly case, since abnormal parenchymal opacities may develop later. seen within the and main bronchi in drowned individuals Patients with obvious pulmonary symptoms with normal initial [27,28] (Figure 4).On post-mortem CT study in drowned radiographs have been documented.

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Central Bringing Excellence in Open Access Brain There are complex mechanisms involved in causing the brain damage from drowning with hypoxia and ischemia being A) B) the primary contributory factors. Hypoxic-ischemic insult cause different injury patterns in infants, older children and adults. Imaging appearance also depends on the severity of the insult. Severe in infants causes involvement of basal ganglia, thalami, brainstem and perirolandic cortex. Relative sparing of thalami and perirolandic cortex is seen in children

Figure 2 45-year-old female with ground-glass opacities and interlobular septal thickening after non-fatal drowning. CT of the between 1 and 2 years of age with severe asphyxia [36]. chest, lung window image reveals “crazy paving” pattern in the bilateral lungs.

Associations between “Takotsubo” or stress cardiomyopathy and near-drowning syndrome have been suggested. A stressful sympathetic nerve activation and massive catecholamine release thatsituation may inducelike a near-drowning left ventricular episode wall dysfunction may result and in chestsignificant pain, mimicking an acute myocardial . Echocardiogram A) B) in such patients reveals left ventricular enlargement and abnormal wall motion, with an apical ballooning pattern as Figure 3 49-year-old female with bilateral pneumothoraces after well as electrocardiogram changes typical for Takotsubo non-fatal drowning episode. Figure 3a: frontal chest radiograph shows dense consolidation throughout the bilateral lungs, in addition cardiomyopathy [29-31]. Experimental animal models have to bilateral pneumothoraces. Figure 3b: CT of the chest at the level of demonstrated massive release of catecholamine in drowning, the aortic arch show extensive pulmonary consolidation and bilateral associated with severe myocardial necrosis [32]. pneumothoraces (arrows). Paranasal sinuses and mastoid air cells Fluid in the paranasal sinuses and bilateral mastoid cells is reported in all fatal drowning subjects. In some of them high attenuation material has been noted layering in the dependent portion of the maxillary and sphenoid sinuses on CT, consistent with inhaled high-density sediment [3,25] (Figure 5). In our

theexperience, different this paranasal is also cavities,a common particularly finding on in CTthe of sphenoid the head and in A) B) maxillarynon-fatal drowningsinuses. victims, with air-fluid levels detected within Figure 4 Abdomen fatal drowning episode. Figure 4a: CT image of the upper chest shows 12-year-old girl with tracheobronchial fluid after a non- opacities. Figure 4b: Mediastinal window, axial image at a lower level an air-fluid level in the trachea (arrow) and patchy parenchymal withProbably high attenuation the most common content abdominal and distended finding stomach in drowning (89% and near-drowning victims is increased amount of gastric fluid shows right lower lobe atelectasis with endobronchial fluid (arrow). of cases) [25] (Figure 6a).Occasionally, high density within the pneumomediastinumgastric lumen, reflecting and aspirated pneumothorax, sand or free sediment air may can be seen also be appreciated on plain films [3]. In patients with extensive extendingAbdominal into thevisceral peritoneal involvement cavity [26]. in near drowning victims is rare, but cases of acute kidney injury with acute tubular necrosis and multisystem organ failure have been documented [33]. In a series of 30adult patients with near-drowning episodes, Spicer et al reported 50% developing acute kidney injury [34,35]. Fluid A) B) overload during resuscitation, as well as acute failure and acute kidney injury may be responsible mechanisms for the Figure 5 23-year-old female with non-fatal drowning episode. CT

bilateral maxillary sinuses (Figure 5b). presence of periportal edema identified on the abdominal CT in shows air-fluid levels (arrows) within the sphenoid (Figure 5a) and some patients (Figure 6b and 6c). J Trauma Care 3(3): 1026 (2017) 4/8 Sannananja et al. (2017) Email:

Central Bringing Excellence in Open Access Severe insult in older children and adults causes involvement Additional indicators of poor outcome (death or persistent of basal ganglia, thalami, sensorimotor cortex, visual cortex, vegetative state) were high signal in the basal ganglia on T2- cerebellum and hippocampi [37,38]. weighted images and abnormal signal intensity in the cortex Mild to moderate insults cause involvement of the watershed zones (regions between the anterior cerebral and middle cerebral correlationon T2-weighted with patientimages outcome(69% sensitivity, seems to be100% in days specificity) 3 to 4, when and arterial territory and between middle cerebral and posterior anbrainstem abnormal infarcts MR imaging (25% examsensitivity, has a positive100% specificity).The predictive value best of cerebral arterial territory). Both cortex and white matter are 100% for persistent vegetative state or death [47]. involved [39]. CT shows diffuse loss of gray-white differentiation, effacement Cervical spine of the cerebral sulci and decreased density of basal ganglia and Drowning and near-drowning victims may present associated other structures (Figure 7). Up to 80% of initial CTs are normal traumatic injuries to the skull, facial bones, cervical spine, , [40] (Figure 8). Occasionally basal ganglia hemorrhagic infarction pelvis and extremities. In a series of 143 children involved in may occur, but usually several days after the acute event. A submersion episodes, Hwang et al reported 4.9% prevalence of “reversal sign” can be seen within 24 hours, which appears, as traumatic injuries, all in the cervical spine. This type of injury increased attenuation of white matter in comparison to the gray matter. The possible explanation of this sign is partial venous outflowThe obstruction “white cerebellum from increased sign” isintracranial another imagingpressure feature[41]. described with severe hypoxic injury, which is seen as increased attenuation of brainstem and cerebellum relative to the cerebral hemispheres. Redistribution of blood to the posterior circulation is a possible explanation for this appearance [42]. A) In survivors, global parenchymal loss with ventriculomegaly B) and widened subarachnoid spaces is noted, usually after the second week [43]. CT has a strong predictive value for patient outcome and residual neurologic injury. Patients with an abnormal initial CT usually have worst prognosis, with higher mortality, permanent neurological damage or persistent vegetative state. developed abnormalities on a later CT examination. In a study Outcome is similarly poor for patients with a normal first CT who C) 100% mortality amongst patients with an abnormal initial CT, D) andof 156 54% children in those with who submersion developed injury,abnormalities Rafaat etafter al., a reported normal initial CT, with 42% presenting persistent vegetative state [40]. Figure 6 Contrast enhanced CT of two different patients with near

On MRI, diffusion weighted sequence shows the earliest in the bottom of a swimming pool by his sister who performed drowning. Figure 6a: 6-year-old boy with gastric fluid, found on the ADC map in the same locations suggestive of diffusion findings with high signal in the injured regions and low signal 30-year-oldcardiopulmonary male withresuscitation. periportal CT edema of the after abdomen a non-fatal shows drowning fluid in restriction. High signal on the diffusion-weighted images peak at the gastric lumen and mild periportal edema. Figure 6b and 6c: week which is known as “pseudonormalization”. T2-weighted theepisode. stomach Contrast as well enhanced as bibasilar CT pulmonaryshows low-density opacities. fluid tracking the and3-5 days FLAIR and sequences then starts become to become positive normal after by the 24-48 end hoursof the first and intrahepatic portal veins (arrows). Low-density fluid is also noted in demonstrate increased signal. Cortical laminar necrosis is seen in the chronic stage with increased signal intensity on the T1- weighted images [44]. Imaging appearance of hypoxic-ischemic encephalopathy is different in preterm and term neonates; however drowning is a rare cause of hypoxic ischemic injury in this age group (Figure 9) [45]. MR spectroscopy (MRS) is another imaging modality for the detection of hypoxic-ischemic injury. MRS is more sensitive

N-Acetyl-Aspartate/Creatinefor injury than other MR imaging ratio in sequences 75.8% and in thepresence first 24 of A) B) hours [45]. Most common MRS findings include a decrease of encephalopathy after a near-drowning episode, generalized / Figure 7 occipitallactate in edema 65.5% had [46]. the Instrongest a series correlation of 22 children with poor with outcome. hypoxic contrast CT of the head shows diffuse loss of gray-white differentiation and cortical 26-year-old sulci consistent female with with cerebral non-fatal edema. drowning episode. Non-

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Central Bringing Excellence in Open Access is particularly prevalent in near-drowning victims when the predominant mechanism of injury was diving. When considered across all ages the prevalence of cervical spine injury in drowning and near-drowning victims is low (less than 0.5%), but the injury more commonly affects the lower cervical spine between C4incidence and C7 is significantly [48,49].In non-fatal higher in drowning adolescents victims, (5%). This a complete type of -up for the cervical spine injury should be obtained if there is concern for a diving accident (Figure 10). Lavelle et al reported bathtub near-drowning victims, including bruising, fractures and a history or findings of abuse or neglect in 63% of pediatric retinal hemorrhage [50]. A) B) SUMMARY/CONCLUSION Imaging plays a paramount role in the initial evaluation as well as monitoring treatment response of near-drowning imaging modality, and typically reveals perihilar bilateral victims. A chest radiograph is commonly obtained as the first hypoxia which more commonly affects the basal ganglia, thalami, brainstem,pulmonary opacities perirolandic that andtend sensorimotorto resolve in the cortex first week. manifest Brain on CT by diffuse loss of gray-white matter differentiation, and by high signal intensity in the injured region on T2 weighted D) sequences, diffusion weighted MRI, and FLAIR, with some C) variation depending on patient’s age. In those cases, in which the mechanism of injury includes diving, careful examination of Figure 9 11-month-old male with anoxic brain injury after drowning. the cervical spine should be part of the imaging protocol. Near Figure a: Axial FLAIR MR image shows hyperintensity in the bilateral basal ganglia, thalami and occipital lobes suggestive of anoxic brain injury in a child who suffered a non-fatal drowning episode. Figures drowning can present with varied imaging findings involving b and c: Axial diffusion-weighted sequence and ADC map image demonstrate diffusion restriction in the bilateral posterior parietal regions suggestive of anoxic brain injury.

A) B)

D) Figure 10 23-year-old male with diving accident and non-fatal drowning episode. CT of the cervical spine shows oblique displaced

posterior fracture fragment into the spinal canal. fracture through the C6 vertebral body with retropulsion of the C) D) multiple organ systems, familiarity with imaging appearances is important to ensure prompt diagnosis and management. Figure 8 30-year-old male with non-fatal drowning episode. Figures a and b. Initial CT of the head at admission shows minimal loss of REFERENCES gray-white matter differentiation. Figure c and d. Follow-up CT 1. obtained four days later shows progressive loss of differential density Geneva, Switzerland. 2008. between the gray and white matter both at the centrum semiovale and Peden MOK, Ozanne-Smith J. World report on child injury prevention gangliobasal regions. 2. radiographs of near-drowned children. Pediatr Radiol. 1985; 15: 297- Wunderlich P, Rupprecht E, Trefftz F, Thomsen H, Burkhardt J. Chest J Trauma Care 3(3): 1026 (2017) 6/8 Sannananja et al. (2017) Email:

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Cite this article Restrepo CS, Ortiz C, Singh AK, Sannananja B (2017) Near-Drowning: Epidemiology, Pathophysiology and Imaging Findings. J Trauma Care 3(3): 1026.

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