The role of the ophthalmologist has been ever-changing, focusing on improving eye health and subsequently a patient's quality of life. The eyes are a valuable source of clues to the state of one's health, aiding clinicians in the study and management of major systemic diseases.1 Beyond its role in life, the eyes have been used to assist with investigations in the field of forensic pathology.2
Forensic pathology focuses on the examination of deceased individuals to assist in the determination of the cause and manner of death, playing an important role in the legal system.3 There are areas in ophthalmology and forensic pathology which have crossed paths historically and areas that may be usefully explored for future options.
The different components of the eye allow a variety of ways of assessing the process and estimation of the time of death. Dilatation of the iris and pupil and clouding of the lens are well-known investigative elements.4–12 Fundoscopy of the retina in the eye has been used to assist in the identification of retinal hemorrhages but the utilization of post-mortem fundoscopy and histological correlation still requires further investigation.2,13 Additionally, post-mortem ocular examination may aid in determining the cause of death and provide clues regarding the length and severity of multisystem disease processes in certain cases.14,15 Post-mortem findings may also assist in the identification of visual impairment conditions which could have contributed to an individual's demise, for example, road traffic accidents or other accidental deaths.16
Post-mortem changes vary for each of the different components of the eye, and some elements may prove useful in forensic pathology. Particular focus will be given to post-mortem iris recognition, post-mortem measurement of vitreous compound levels, the retina in pediatric abusive head trauma, and the use of ophthalmic imaging such as optical coherence tomography (OCT) to aid diagnosis of the condition, as we recognize these areas have shown potential for routine implementation in practice and/or necessitate further exploration before routine use.
MEDLINE, Embase, and PubMed were searched to identify potentially eligible articles pertaining to forensic ophthalmology up till 3 June 2021. The following search terms were used:
- a) Keywords (all fields): forensic pathology OR postmortem OR post-mortem OR autopsy; ophthalmology OR eye OR shaken baby syndrome;
- b) the following medical subject heading (MeSH) terms in MEDLINE and Embase: forensic pathology OR post-mortem change OR autopsy; ophthalmology OR eye OR vitreous body OR retina OR lens or pupil OR pupil reflex OR shaken baby syndrome OR retina hemorrhage OR head injury OR brain hemorrhage OR child abuse;
- c) the following MeSH terms in PubMed: forensic pathology OR autopsy OR change, postmortem; ophthalmology OR abnormality, eye OR abnormalities, eye OR body, vitreous OR bodies, vitreous OR lens, crystalline OR abnormal pupillary function OR iris OR brain hemorrhage OR head injury
Articles were eligible if they explored ophthalmological post-mortem changes and/or the use of ophthalmological post-mortem changes in forensic pathology. Articles not in the English language were excluded. Additional articles and sources including books and online publications were found by consulting experts in the field and reference list in articles. Conference abstracts were used if they were referenced in articles. If full-text articles were not available, or abstracts were not available in the English language, they were not cited but mentioned as a secondary source. From a total of 890 articles or conference abstracts found, 104 articles were selected for our review. A further 9 books and 5 online publications were used.
The cornea is a transparent avascular tissue, with various factors contributing to its transparency, including the regular and uniform arrangement of corneal epithelium, lamellar arrangement of collagen bundles in the corneal stroma, intracellular junctions, tightly controlled hydration of normal cornea, and corneal avascularity.17 Morphological changes in the cornea during the post-mortem interval (PMI) are well-known phenomena, with descriptions in the literature dating back to the 1840s.4,5
After death, the loss of the corneal reflex is used as a criteria for brainstem death.19 Various studies have reported a correlation between corneal turbidity and PMI.6 While there has been a mix of subjective examiner judgment and objective measures used to improve accuracy in assessing corneal turbidity (Aoki, cited in Kawashima et al7), more recently there have been efforts to use computer image analysis technology to quantify corneal opacity and estimate PMI using rabbit corneas.8
Using optical coherence tomography (OCT), Napoli and colleagues studied sheep corneas and detected a variety of architectural changes in different phases post-mortem.9,20–23 They reported that the anterior and posterior stroma behaved differently.9 Observing post-mortem corneal changes, Nioi et al discovered that there was a reflectivity differentiation between the anterior and posterior stroma,9 which was later also found in human corneas.24 Supporting these findings is a study by Muller et al, which reported the relative rigidity of the anterior stroma compared to posterior stroma in human corneas in various hydration states.10
Napoli and colleagues demonstrated the feasibility of a portable spectral-domain OCT (SD-OCT) system (iVue SD-OCT, Optovue Inc, Fremont, CA, US) in detecting central corneal thickness variations in sheep corneas and human corneas at different phases after death.20,24,25 There has been preliminary investigations in human corneas using portable OCT—authors discovered the formation of stromal waves in the posterior stroma of corneas from the third hour of death which they have termed “Nioi-Napoli sign”, possibly representing a novel sign for PMI estimation.9,24,26
In recent human corneal studies using OCT, Nioi and colleagues also detected a gradual decrease in the amplitude of the anterior chamber and changes in the corneal curvature, with eventual full iridocorneal contact, loose corneal sphericity, and anterior chamber abolition.24
The lens contains two kinds of fiber cells: those in the cortex and those in the nucleus. The cells in the cortex are immature, still containing organelles which are degraded, leaving behind membrane-enclosed bags of crystalline. Cells in the nucleus are mature and display an absence of organelles.27,28 The post-mortem loss of lens transparency is attributed to the metabolic processes that occur, alongside cell necrosis.28 After death, a halt in active transport causes the epithelium to accumulate potassium, and subsequently calcium and chloride. The resulting oxidizing agents cause linkage and aggregation of proteins, resulting in opacification of the lens.28–30 These biochemical changes identified above represent a possibility of using the lens to assist in establishing the PMI. However, along with the scarcity of research in this area, its practicality is a barrier to implementation of this method as there can be a delay between the time of death and time body is found and/or post-mortem examination.
Studying enucleated rabbit lenses, Prieto-Bonete and co-workers reported that macroscopically, the lens was visibly cloudy from 72 hours post-mortem, and by 96 hours, it became opaque.28 The spherical structure of the lens also degenerated over time due to fluid influx and separation of the lens fibers. Histologically, at 24 and 48 hours all the cell layers (external capsule, cortex, epithelium, nucleus) were visible but after 72 hours, changes in the structure and order of the cell layers started to appear; and at this point, it was not possible to visualize the capsule or epithelium, and the fibers of the cortex and nucleus were disaggregated and separated. At 96 hours, aggregated eosinophilic structures are seen.28
Iris and Pupils
Physiologically, the iris react in two ways, either by dilating due to dilator pupillae muscle contraction or by constricting due to sphincter pupillae muscle contraction.31 A dilated pupil, unresponsive to light is considered a critical sign in acute neurology and neurosurgery.32 It is also an axiom that a fixed dilated pupil occurs ipsilateral to a space-occupying lesion exerting a mass effect with raised intracranial pressure.33
First experimentations studying this pupil abnormality date back to the 1800s and work in 1900s,32 and authors have speculatively attributed the ipsilateral dilated pupil to the stretching of the oculomotor nerve over the clivus, or by compression by buldging hemispheric mass or hemorrhage.32 Furthermore, there can be a false-localizing impaired reaction in the contralateral pupil, but its pathophysiology has not been resolved.32 Despite the wide use of the iconic “fixed and dilated pupils” sign in medicine, its underlying mechanisms remain debatable.32,33
The formal diagnosis of death varies between countries, but most definitions involve the irreversible loss of brain function with pupil size and/or reactivity being included as diagnostic criteria.34 Pupil appearance and reaction are used as a criterion to diagnose death, but there are discrepancies to how it is used in various countries.11 In Australia, New Zealand, and Japan, bilateral unreactive pupils with diameters of > 4 mm is used as a criterion.12,34 On the other hand, in the UK, for brain death diagnosis, pupils are not required to be > 4 mm, only that they are fixed and are unresponsive to the alterations in incident light intensity.35 The guidance in the United States and Canada states that pupils are typically dilated or midsized after brain death but does not stipulate that pupil diameters have to be > 4 mm 36,37
Intriguingly, the precise mechanism of mydriasis in brain ischemia and anoxia is uncertain, but the loss of third cranial nerve tone and parasympathetic inhibition are among postulated mechanisms. Furthermore, one can ponder whether a minimum pupil size as a prerequisite for the diagnosis of brain death is necessary.11 In the process of developing the Japanese criteria for brain death, variations in the size of pupils were found in patients with suspected brain deaths, and approximately 20% of these patients had a pupil diameter <4 mm.12
During life, exogenous substances, such as alcohol, opioids, etc can affect the eye in a variety of ways, including causing a change in pupillary size and pupillary reaction to light.38 However, these changes may or may no longer be apparent after death.18
Spontaneous post-mortem changes in pupil size have been described to follow a chronological sequence by numerous studies using experimental animal models and in post-mortem human observational studies. However, results have been tainted with discrepancies.39
Some authors reported miotic changes only;40 some reported initial miosis followed by mydriasis, while some described three phases of miosis-mydriasis-miosis.39 The methodology of measuring pupil size has not been standardized and may include scales,40 optic pupilometer (Willer, cited in Fleischer et al 39), at times modified using a keratometer (Klein, Prokop, cited in Fleischer et al39) and tape measure.41 The reliability of these measurements have not been published39 and some publications did not report the methods used (Placzek, Ritter, cited in Fleischer et al).39
Post-mortem pupil size changes to estimate PMI have been investigated. Fleisher and colleagues assessed spontaneous post-mortem changes in pupil width in humans using computer-assisted analysis of digital images of the pupil-iris region, which they found to have excellent intra- and inter-rater reliability.39 The authors reported that while statistical approximation of the time course of pupil-iris ratio (PIR) demonstrated a pattern of initial miosis in the first 12 hours post-mortem, they do not recommend that spontaneous post-mortem changes in pupil width should be used in estimating PMI due to large variations in PIR between single cases over time.39
Another approach of interest in estimating PMI is by using the iris’ supravital reaction, which is the body's response in the early post-mortem period as some organs or cells do not immediately die after death.42 Researchers discovered that pupillary reaction to pharmacological stimulation continues for hours after death, up to 20 hours (Schleyer, Bardzik cited in Larpkrajang et al)43 but more recent studies in this area have been divergent. A study concluded that pupillary reaction to pilocarpine had a statically significant correlation to PMI, and proposed that use of change in the pupil size after pilocarpine administration in a regression equation could be used to predict PMI.43 However, another two studies determined that positive, negative, and paradoxical responses in stimulated irises can be obtained, meaning any conclusions made could be misleading.41,44
Overall, the correlation of pupil size with PMI and its mechanisms is still not well established. Strikingly, the discrepancies in the sequence of post-mortem pupil width changes found by various authors bring us to an intriguing question, which is whether or not the finding of dilated pupils post-mortem is nothing but an urban myth.
Another area in which the iris appearance is useful in forensic medicine is in the field of biometrics, the science of identifying individuals based on their characteristics.45 Biometrics have been used in law enforcement for as long as they have been studied.46 The most common biometric identifiers include fingerprints, hand geometry, and face, voice, and iris recognition.46,47
The iris has patterns that are unique to each individual and are even distinct between an individual's left and right eye and between identical twins, making it more biometrically distinct than DNA and therefore an excellent candidate for biometric use.48 Iris recognition technology is currently widely implemented in life, for access control and identification purposes.49 However, iris recognition after death, possibly due to post-mortem changes in the eye,7,50–52 may result in deterioration of its algorithm accuracy.50 The period of viability of the iris is dependent on environmental conditions, with iris biometric data obtainable up to 4 days post-mortem in warmer seasons to more than 50 days in winter.52 It has been shown that post-mortem iris recognition of bodies kept in mortuary conditions was possible 5 to 7 days after death, and occasionally up to 21 days.53
It appears that there is some evidence for the viability of post-mortem iris recognition, particularly under favorable conditions, possibly reflecting an area of research that would benefit from further evaluation in larger numbers with different biometric technologies as well as assessment under different environmental conditions. The addition of routine use of iris biometrics to an individual's e-passport and verification of the reliability of this technology in death would greatly assist the forensic pathologist in the identification of individuals post-mortem.
Other Anterior Segment and Ocular Changes
Findings such as subconjunctival hemorrhage may indicate direct ocular trauma, or as a result of a sudden increase in intrathoracic pressure from blunt trauma to the thorax, severe vomiting, Valsalva maneuver, or paroxysmal coughing, a likelihood that is increased in the presence of coagulopathy. Scleral lacerations, globe ruptures, hyphaema, lens dislocation, periorbital ecchymosis have several causes but may suggest a more sinister cause of death, such as abuse or homicide.54,55
If eyelids remain open after death, triangular-shaped areas of scleral discoloration known as tache noir (meaning “black spots”) are seen, which are due to desiccation.19 These may be yellowish initially before becoming brown and later black, potentially giving an artefactual appearance of subconjunctival hemorrhage.18 Recently, using OCT (iVue SD-OCT, Optovue Inc, Fremont, CA, US), scleral tache noir was observed as a three-dimensional structural image, characterized by hyper-reflectivity of the outer layer, along with physical separation between the choroid and sclera.24 After death, there is a drop in intraocular pressure as the arterial blood pressure is absent, causing the eyes to look sunken and feel softer. Nicati reported that no tension is left in the eye 2 hours after death (Nicati, cited in Saukko and Knight)18 and Balci et al reported a progressive reduction in intraocular pressure, postulating that it can be useful in PMI estimation.56
The post-mortem chemical and biochemical analysis of bodily fluids, termed thanatochemistry, is a useful tool in forensic investigation.57 The vitreous is particularly useful in investigating deaths related to ketoacidosis (alcoholic or diabetic) and hypothermia.13
The vitreous has served as an alternative matrix to other biofluids for more than 50 years.58 Located between the crystalline lens and retina, the vitreous is a unique and useful alternative matrix in forensic toxicology due to its relative isolation from other body compartments owing to the blood-retinal barrier (BRB), which restricts diffusion, secretion and filtration of materials, thus protecting it from bacterial contamination due to its limited vascularisation.57 Compared to the use of blood and cerebrospinal fluid, the use of vitreous humor is advantaged by its accessibility, ease of sampling, less susceptibility than blood to rapid chemical change, and relative independence from environmental influences and is less subject to putrefactive changes.57,59
The vitreous is almost entirely composed of water (99%) and contains carbohydrates such as glucose, lipids and electrolytes such as potassium, sodium, lactate, chloride and ascorbate, along with proteins, hyalocytes, hyaluronic acid, and collagen fibers.59 Specific solutes are transferred beyond the BRB via active transport, but for some solutes, this occurs by passive diffusion, achieving a vitreous concentration close to that of plasma.59,60 However, in the initial period after death, the rate of exchange of organic endogenous small molecules and ions between vitreous and blood circulation decreases.57
As vitreous humor is viscous, it often requires pre-treatment such as centrifugation, heating, dilution, or the addition of hyaluronidase to facilitate accurate pipetting.61 Nonetheless, there is a current lack of analytical methods developed specifically for vitreous. There is also the possibility of water loss from the eye with time since death and body storage conditions, which leads not only to increased vitreous humor viscosity but also increased analyte concentrations.13 Concurrent or past eye diseases (eg, retinal detachment, surgical manipulation, or posterior chamber disease) may affect the vitreous humor.62 Other circumstances such as the environment in which a body is found, such as immersion in water, must also be taken into account.63
Various biochemical constituents of vitreous, including potassium, lactate, glucose, ketone, acetone and beta-hydroxybutyrate, have been most frequently studied in relation to post-mortem forensic applications and will be discussed below.
Among the ions of interest in vitreous post-mortem biochemistry, potassium is one of the most researched.64 In vivo, there is active transport of potassium into the posterior chamber across the ciliary body and through the lens anterior capsule and passive diffusion through the posterior capsule of the lens into the vitreous body, resulting in a slightly higher potassium concentration in vitreous than in the plasma.64
After death, active membrane transport and selective membrane permeability cease, leading to gradual leakage of potassium out of cells and into the surrounding extracellular fluid. Numerous studies over the years, with a large variability in methods used, have shown vitreous potassium as potentially useful in determining the PMI.57 However, there is a potentially biphasic rise in vitreous potassium post-mortem resulting in a widening of the confidence interval at high PMI, thereby affecting the reliability of the results.57 There are various formulas suggested by authors but factors such as environmental temperature, agonal period and elements relating specifically to the deceased (eg, body size, age, and concurrent pathology) may affect vitreous potassium levels. Therefore, vitreous potassium levels are not routinely used to determine the PMI in current forensic practice.57
Glucose and lactate
Glucose plays a central role in cell metabolism and it is often analyzed in suspected cases of hypo- or hyperglycemia to aid diagnosis. Vitreous glucose levels are often lower than in blood.13 In the post-mortem period, glycolysis continues, causing an initial decrease in vitreous glucose concentration, but in the next few days, remains fairly stable while lactate levels gradually climb through anaerobiosis.57 Therefore, low vitreous glucose cannot be taken to infer hypoglycaemia.57
In forensic practice, a high vitreous glucose concentration may indicate hyperglycemia associated with diabetic ketoacidosis, hyperosmolar non-ketotic hyperglycemia or another cause such as in association with cerebral hemorrhage, congestive heart failure, electrocution, hypothermia, and cardiopulmonary resuscitation where vasopressors and glucose may be administered.57 Hockenhull and colleagues suggested that high vitreous glucose concentrations occurring alongside a substantial rise in beta-hydroxybutyrate may be used to discriminate deaths due to diabetic ketoacidosis from ketoacidosis caused by other circumstances.65
Ketone bodies, beta-hydroxybutyrate, and acetone
β-hydroxybutyrate is considered to be most specific as vitreous marker of ketoacidosis, preferred over vitreous acetone.57,65 However, it is recommended that when elevated acetone is detected in vitreous, ethanol and glucose assays should be run to differentiate alcoholic ketoacidosis and diabetic ketoacidosis.66
Post-mortem vitreous sodium, chloride, and magnesium have also been investigated, but an inconsistent correlation has been found between these compounds and PMI. Fructosamine, which appears to be protected from post-mortem autolytic phenomena, was found to be 3.09 times elevated in diabetics compared to non-diabetic subjects. Additionally, the substantial correlation was found between vitreous fructosamine with glucose levels, making it a plausible indicator of diabetes in the antemortem period.57
Countless numbers of other biochemical compounds in the vitreous have been investigated, including ammonium, magnesium, amino acids, creatinine, creatine, urea, lactate dehydrogenase, creatinine-kinase myocardial band, N-acetyl-cystein-activated creatine kinase, liver enzymes (alanine aminotransferase, aspartate transaminase, gamma-glutamyl transferase), chorionic gonadotropin, insulin and insulin analogs, carbohydrate-deficient transferrin, hypoxanthine,13,57 zinc,67 aminopeptidase,68 and hormones,69 which we will not discuss in detail here. Vitreous humor is a useful substrate for post-mortem toxicological analysis (especially alcohol as well as other drugs) and has been thoroughly covered in other reviews.70,71
Metabolomic approach in the vitreous
Metabolomics is the quali-quantitative study of the low-molecular-weight metabolites in a biofluid or tissue and their changes with any pathophysiological stimuli, including death.72 Recently, based on studies in animals, hydrogen-1 nuclear magnetic resonance metabolomics have been found to be able to detect post-mortem changes in metabolite profile of vitreous and aqueous humor, and therefore have been proposed as a PMI estimation tool.72–76
Point-of-care testing technology
Point-of-care (POC) testing for glucose and ketone bodies in blood or urine is widely used for monitoring diabetes in the form of a semi-quantitative stick test77,78 or a test strip used with electrochemical monitoring devices.78–81 Vitreous ketone bodies and glucose can also be measured to assess antemortem hyperglycemia and ketoacidosis,57,65,82,83 as an alternative to more costly analytical methods such as gas chromatography.79,84
Use of POC testing in the mortuary to evaluate vitreous glucose and ketone bodies has garnered interest. However, results showed a tendency of the blood glucose monitoring system to overestimate the glucose concentration, suggesting it may be useful as a primary screening tool in the mortuary, aiding the post-mortem detection of hyperglycemia and ketoacidosis, before following up with subsequent analytical methods for confirmation.79
The retina, a structure composed of layers of specialized neurons and vascular networks,85 is a unique site where the condition of the microcirculation can be non-invasively imaged, and it has been shown to provide information predicting the risk of coronary heart disease.86 As an extension of the central nervous system (CNS), the examination of the eye can be a non-invasive approach to the diagnosis of some CNS diseases.85
Immediately after death, a phenomenon termed retinal vessel segmentation, or “trucking” (also called Kevorkian sign), takes place.87 The continuous blood column in the retinal blood vessels breaks up into small segments which then collide with each other. The retina also develops increasing pallor as PMI increases. The disc outline becomes hazy after a few hours.88
Examination of the retina post-mortem is vital in certain forensic circumstances and most importantly in the detection of retinal hemorrhages in pediatric cases. The role of retinal examination in abusive head trauma is well documented and continually being examined, discussed, and investigated. Facial and skeletal injuries can be found in cases of non-accidental injuries as well as a wide spectrum of ocular injuries, including subconjunctival hemorrhage, chemosis, periorbital edema, corneal epithelial loss, hyphaema, and globe rupture89,90—but focus will be given to the retina in the following section.
The retina in abusive head trauma
Retinal hemorrhages were first described in association with child abuse in 1928 by Aikman (Aikman, cited in Levin et al).91 Retinal hemorrhages were then identified as part of a constellation of injuries, including intracranial and intraocular bleeding and fractures, which was termed “shaken baby syndrome” and described abusive head injuries in infants sustained as a result of violent shaking with or without blunt head impact.92 The term “Whiplash Shaken Infant Syndrome”93 was then described, but abusive head trauma or non-accidental head injury is a more comprehensive term reflecting the brain injuries that children suffer as a result of abuse and includes shaking as a mechanism of injury with or without impact, impact alone, crushing injuries or a combination of several mechanisms.94
The mechanisms underlying retinal hemorrhage from abusive head trauma are still not clearly established, with two main theories debated in the literature. The first theory postulates vitreoretinal traction as the cause, ascribed to forces of deceleration from impact and/or shaking.95 The second theory postulates that impaired venous return from the eyes due to increased intracranial pressure from intracranial hemorrhage and brain edema or increased intrathoracic pressure, for example, from chest compression, rib fractures, results in retinal hemorrhage.96
Numerous types of ocular, periocular, and orbital injuries have been described in child abuse, but retinal hemorrhages are the most frequent ocular manifestation of abusive head injury, observed in approximately 75% of abusive head trauma cases, with studies reporting a range of 50% to 100%.97 A systematic review of 62 studies assessing retinal signs to distinguish abusive head trauma from non-abusive head trauma found that in a child with head trauma and retinal hemorrhage, the odds ratio that this was abusive head trauma is 14.7 (95% confidence intervals: 6.39 to 33.62) and the probability of abuse is 91%.98
There appears to be an association between the severity of retinal hemorrhage and the severity of neurological injury, with the highest frequency of retinal hemorrhages seen in autopsy cases and lowest in neurologically normal survivors.99,100 Hemorrhages are typically found in bilateral eyes, although substantial unilaterality or asymmetry is not uncommon and does not appear to be related to its diagnostic significance.101 Laterality of retinal observations has not consistently been found to correlate with laterality of intracranial findings.102
Retinal hemorrhages can vary in type, location, size, and severity. Most studies described hemorrhage in all the retinal layers103; but numerous studies reported more frequent and heavier involvement of the superficial layers including the sub-internal limiting membrane, nerve fiber layer and ganglion cell layers.103 Retinal hemorrhages may be located in the peripapillary area, posterior pole, peripherally and the ora serrata.54 However, the posterior pole of the fundus is the most frequently reported location of intraocular hemorrhage.103 Vitreous hemorrhage though rare, can be seen as well.100 Pre-retinal hemorrhages and vitreous hemorrhage were more frequently reported in post-mortem rather than clinical series.103
It should be noted that retinal hemorrhages can occur in newborns as a consequence of birth. They are seen in around a quarter of normal deliveries and with an increased frequency in instrumental deliveries, but they rarely persist beyond 6 weeks.104 Therefore identification of retinal hemorrhages in a child beyond the neonatal period should raise questions relating to the potential of concurrent disease or the possibility of non-accidental injury. In children with intracranial hemorrhage, the presence and increasing severity of retinal hemorrhages are associated with increased odds of abuse rather than accidental injury, particularly in children younger than 6 months of age.105
A systematic review of studies of abusive head trauma with case definition provided by the third-party witness, confession, multidisciplinary assessment or legal decision was conducted by Bhardwaj and colleagues in 2010. The review also studied other conditions such as motor vehicle crashes, sudden infant death syndrome, central nervous system diseases, and other unexplained deaths.103 Intraocular hemorrhages were discovered in 74% (range: 51–100%) of clinical cases and 82% (range: 63–100%) of autopsy cases. Contrastingly, intraocular hemorrhage was found in 6% of accidental head injuries and was reportedly mild in severity. The authors concluded that the overall sensitivity and specificity of intraocular hemorrhage for abusive head trauma was 75% and 94% respectively. Posterior pole intraretinal hemorrhage was the most common finding for abusive head trauma cases but extensive, bilateral and multi-layered intraocular hemorrhage was the most specific.103
Perimacular folds, white retinal ridges surrounding the macula,106 and macular retinoschisis, splitting of the retinal layers95 are associated with more severe neurologic injury and high mortality.103,107 They are considered specific but not pathogonomic findings for abusive head trauma, as they, although extremely rare, may occur in other conditions.103
Ophthalmological assessment of retinal hemorrhages and opinion of their cause should not be based on the presence of hemorrhages alone, but on the entire clinical picture.108 The absence of retinal hemorrhages does not preclude the mechanisms of non-accidental head injury or shaken baby syndrome.109
Use of fundoscopy and imaging technology
In some suspicious trauma or pediatric cases, post-mortem assessment of the fundus has relied on ocular enucleation to aid with the diagnosis of the cause of death.16 Recently, post-mortem ophthalmic endoscopy and monocular indirect ophthalmoscopy have been described, and although not currently routinely used, may prove useful in the initial examination of the eye in forensic autopsy cases110–113 as eye enucleation can result in artifacts.114 The instant endoscopic inspection and documentation of the fundus in forensic autopsies may be further beneficial for practical reasons, to justify post-mortem enucleation of the eyeball which is restricted in some countries in the presence of pathological findings.111 Photographs of the retinal findings provide supportive evidence and is a useful part of patients’ records.109
Lantz et al115 highlighted the potential for smartphone still-image capture techniques and video-sequence recording during post-mortem monocular indirect ophthalmoscopy without the use of a retinal camera.115 Other technologies also recently introduced to clinical practice is the RetCam and the OCT. The RetCam (Clarity Medical Systems, Pleasanton, CA, US), a contact digital fundus camera provides an alternative to indirect ophthalmoscopy for retinopathy of prematurity (ROP) screening. In pilot study of suspected and confirmed clinical cases of abusive head trauma, the RetCam was shown to provide high-quality photographic images for evaluation and documentation of retinal hemorrhages.109 The OCT, which has revolutionized the assessment and management of a wide variety of ocular diseases,116 has contributed to our understanding of the vitreoretinal relationships in abusive head trauma.109 OCT in infants who are victims of abusive head trauma revealed retinal traction, perimacular folds and macular retinoschisis previously not seen by ophthalmoscopy, possibly providing data favoring the theory of vitreoretinal traction in abusive head trauma.117 The hand-held SD-OCT (Bioptigen Inc, Morrisville, NC, US) has also been developed, allowing imaging of a supine infant, and has been successfully used to identify both acute and chronic vitreoretinal findings in live infants with abusive head trauma.109
Post-mortem eyes from autopsy, however, present challenges to standard OCT imaging including clouding of the lens and cornea and standard of care autopsy processing resulting in oblique views to the macula.24,118 McNabb and associates were able to overcome this optical interference of the anterior segment structures and acquire macular images using OCT attached to a custom periscope.118
Ophthalmoscopy, OCT, and the Retcam show potential in assessment of live victims of abusive head trauma but at present, they are not used routinely in post-mortem assessments and studies have highlighted areas of inherent difficulty as a result of post-mortem changes in the eye.118 Nonetheless, this is still potentially an area of investigation.
This review has aimed to highlight the extent and breadth of research into the post-mortem ophthalmological changes which have benefited forensic pathology. Whilst some areas of research have not necessarily translated into current routine forensic practice, they highlight the scope for further research options. As technology advances, so further avenues for the investigation of this area of forensic pathology will continue to open up. The most important areas for further study are in the estimation of post-mortem interval, analysis of ocular biochemistry to determine the cause of death, providing diagnostic evidence for the occurrence of non-accidental head injury in children, and post-mortem identification of unknown decedents using ocular biometrics. The amalgamation of knowledge, skills, and expertise in the areas of both ophthalmology and forensic pathology should continue to advance synergistically to develop our understanding of the eye in death. In doing so, this will contribute to our understanding of forensic ophthalmology, and further assist the pathologist in post-mortem investigations.
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