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Study of endolaryngeal structures by videolaryngoscopy after hanging: A new approach to understanding the physiopathogenesis
Forensic Science International 192 (2009) 48–52
Contents lists available at ScienceDirect
Forensic Science International journal homepage: www.elsevier.com/locate/forsciint
Study of endolaryngeal structures by videolaryngoscopy after hanging: A new approach to understanding the physiopathogenesis S. Duband a,b,*, A.P. Timoshenko c,d, R. Mohammedi e, J.-M. Prades c,d, F.-G. Barral e, M. Debout a, M. Pe´oc’h a,b,1 a
Department of Forensic Medicine, Saint-Etienne University Hospital Center, Bellevue Hospital, 42055 St-Etienne, Cedex 2, France Department of Pathology, Saint-Etienne University Hospital Center, North Hospital, 42055 St-Etienne, Cedex 2, France Department of Otolaryngology-Head and Neck Surgery, Saint-Etienne University Hospital Center, North Hospital, 42055 St-Etienne, Cedex 2, France d Department of Anatomy, Jacques Lisfranc Faculty of Medicine, Jean Monnet University, 15 rue Ambroise Pare´, 42023 St-Etienne, Cedex 2, France e Department of Radiology, Saint-Etienne University Hospital Center, Bellevue Hospital, 42055 St-Etienne, Cedex 2, France b c
A R T I C L E I N F O
A B S T R A C T
Article history: Received 20 October 2008 Received in revised form 16 July 2009 Accepted 21 July 2009 Available online 20 August 2009
Purpose: To evaluate laryngoscopic findings in hanging cases and to compare them with magnetic resonance imaging (MRI) and forensic autopsy results. Materials and methods: Postmortem nasolaryngofibroscopy and MRI of five people who died from hanging were performed. Three people who died from other causes than hanging were also examined with a flexible laryngofibroscope. The results were compared with injuries discovered during forensic autopsy. Results: In all five hanging cases, laryngofibroscopic investigation showed a vocal fold position in complete adduction confirmed by MRI. This position did not seem to be influenced by the intensity of the forces applied to neck or postmortem delay and cadaveric phenomena. The vocal cords of the three nonhanging deceased were found in the intermediate position. These findings could suggest that pressure applied to the cervical nervous and cartilaginous structures or their elongation during hanging could lead to closure of the glottis with vocal cord adduction maintained after death. Conclusion: Laryngofibroscopic examination in hanging cases could be very useful in confirming the vital character of the hanging and understanding asphyxial phenomena in incomplete suspension without laryngeal crush. ß 2009 Elsevier Ireland Ltd. All rights reserved.
Keywords: Hanging Nasolaryngofibroscopy Larynx Vocal cords Vocal cords position Forensic interest
1. Introduction Because there is no pathognomonic sign of hanging, its diagnosis is difficult to categorically establish and is always based on several arguments but can sometimes be uncertain if vital injuries are absent or invisible. Although in current forensic practice, such injuries as soft-tissue cervical hemorrhages or vital fractures of laryngeal skeleton are systematically researched and regularly published [1– 3], the appearance of the endolarynx is never highlighted. Furthermore, the diagnosis of vital signs depends on the techniques used [4]. Several authors currently affirm that multislice spiral computed tomography (MSCT) and magnetic resonance imaging (MRI) offer great potential for the detection of these injuries [5–7]. In the following, magnetic resonance imaging, videolaryngo-
* Corresponding author at: Department of Forensic Medicine, University Hospital Center of Saint-Etienne, 42055 Saint-Etienne, Cedex 2, France. Tel.: +33 (0)4 77 12 05 23; fax: +33 (0)4 77 12 09 16. E-mail address: [email protected] (S. Duband). 1 Tel.: +33 (0)4 77 12 05 23; fax: +33 (0)4 77 12 09 16. 0379-0738/$ – see front matter ß 2009 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.forsciint.2009.07.015
fibroscopy and autopsy findings of five asphyxia fatalities by hanging are analyzed and compared with three non-hanging deceased. The aim of this study was to evaluate the appearance of the endolarynx and the benefit of laryngofibroscopic examination as possible diagnostic tools of hanging in postmortem situations. 2. Materials and methods 2.1. Subjects The responsible justice department approved the present study. Five cases of suicidal hanging described in Table 1 (five males, mean age = 51 years, age range = 33–83) were examined using postmortem pre-autopsy MRI and videolaryngofibroscopy. One case (case 6, male, 25 years), for which autopsy was not required, was only investigated by two successive laryngofibroscopy examinations at 48-h intervals. Three non-hanging deceased (cases 7–9, males, mean age = 54 years) were only investigated by laryngofibroscopy within 24 and 48 h after death (no data being available in the literature) for comparison. All of the corpses were undressed and examined externally prior to scanning and autopsy by a forensic pathologist. The body mass index (BMI), the type of hanging and the link used were recorded. The time since death was evaluated using current standard methods of body temperature, degree of rigor mortis and investigation data. The time of suspension was approximated from the time since death and police and detailed interviews of the relatives of the deceased. The results of the external examination were recorded, e.g. conjunctival congestion or bleeding, cyanosis, visible neck
S. Duband et al. / Forensic Science International 192 (2009) 48–52
49
Table 1 Characteristics of subjects and hangings of study. Case
Age (years)
BMI
Link
Type of hanging
1
48
22.9
Rope
2
33
23.7
Girths
3
33
22.3
4
83
28.4
Electric extension Rope
5
58
23.4
Girths
6
25
19.9
Rope
7 8 9
29 59 75
20.8 26.3 23.2
– – –
Atypical incomplete Atypical incomplete Typical complete Atypical unknown Atypical incomplete Atypical complete – – –
Characteristics of cervical compression
Suspension time (h)
Type of knot
Anatomical position of loop
Anatomical position of knot
Slip knot
Above thyroid prominence Above thyroid prominence Above thyroid prominence Above thyroid prominence Above thyroid prominence Above thyroid prominence – – –
cartilage
Regarding left mastoid
41
cartilage
Regarding left mastoid
12 2
cartilage
No visible print
cartilage
Behind left mandibular angle
cartilage
No visible print
81
cartilage
No visible print
51
– – –
– – –
Slip knot Fixed knot Slip knot Fixed knot Fixed knot – – –
injuries, etc. The bodies were preserved at a temperature of 4 8C after their admission to the forensic department and prior to the different examinations. 2.2. Postmortem MRI and videolaryngofibroscopy The telelaryngoscopy examinations were conducted using a flexible nasolaryngofibroscope Olympus ENF type P4 and conventional video system with microcamera Storz tricam. Images were digitalized using image capturing program E-capture (Metris). For MRI, the bodies were wrapped in artifact-free body bags to prevent contamination of materials. All MR examinations were performed with a 1.5-T system (Intera Achieva 1.5 T; Phillips) and consisted in T1, T2 fast spin-echo (FSE) and short-tau inversion recovery (STIR) sequences with an antneck coil (Neurovascular 8 channel Array head-neck). The mean times between estimated death, laryngofibroscopy examination and imaging were 27 and 38 h, respectively. 2.3. Forensic autopsy A standard autopsy was performed according to current guidelines at an average time of 9 h after imaging. The layer by layer neck dissection was undertaken after evisceration of the other organs following the protocol of Prinsloo and Gordon [8] and the cervical spine was extracted and examined after removal of vertebral body. In all the autopsied cases, samples of each major organ and injured tissue were histologically analyzed after formalin fixation, embedding in paraffin and hematoxylin–eosin–saffron staining. After macroscopic examination, when a fracture was present, the laryngeal skeleton conserving the surrounding adherent soft tissue was decalcified with a 10% HNO3 solution and microscopically examined. 2.4. Data analysis A direct comparison of the imaging, videolaryngofibroscopy, autopsy and histology findings was carried out taking the autopsy and histology data as reference.
3. Results 3.1. Subject and hanging characteristics The main subject and hanging characteristics are summarized in Table 1. In all the hanging cases, the ligature mark on the neck was always above the thyroid cartilage prominence. The causes of death revealed by autopsy and toxicological analysis of blood, urine and gastric content samples of the last three subjects (cases 7–9) were opioid intoxication, myocardial infarct and ballistic intracranial trauma, respectively. 3.2. Comparison of autopsy and imaging findings in hanging cases The results of comparison between autopsy and imaging findings concerning neck structures except for buccal and endolaryngeal elements are shown in Table 2.
71 43 4
Table 2 Cervical findings by MRI and autopsy (N = 5, and the number of the observations is indicated in brackets). Findings
MRI
Autopsy
Subcutaneous hemorrhage Intramuscular hemorrhage Perivascular hemorrhage Fracture of hyoid bone Fracture of laryngeal cartilages Sinusal lymph node congestion Epidural cervical spinal hemorrhage
3 4 1 0 0 3 1
4 4 1 1 0 3 1
[1,3,4] [1,3–5] [4]
[2,3,5] [3]
[1,3–5] [1,3–5] [4]; Fig. 1A [2]; Fig. 1B [2,3,5] [3]
In all cases, the autopsy suggested the asphyxial nature of death and the histological aspect of the lungs were similar and consisted in emphysema (Fig. 1C). In these five observations, hanging was due to suicide attempt. 3.3. Comparison of buccal and endolaryngeal findings on autopsy, laryngoscopy and imaging in hanging cases The results of correlation of laryngofibroscopy, MRI and autopsy findings concerning the endobuccal and endolaryngeal structures are summarized in Table 3. The abundance of secretions found during nasolaryngofibroscopy (performed in all cases before MRI) above the glottic plane required an aspiration system to progress into the laryngeal tract. The posterior placement of the root of the tongue observed in two cases was responsible for complete obstruction of the oropharynx in the median plane (Fig. 2A). The base of tongue congestion (Fig. 2B) gave a cyanic pseudo-ecchymotic aspect to this anatomical region with laryngoscopic examination and hypersignal in T2-weighted MRI. In all cases, vocal cord adduction in the median plane was observed with contact between the vocal processes of arytenoid cartilages (Fig. 3).
Table 3 Endolaryngeal findings at laryngoscopy and imaging examinations and autopsy (N = 5). Findings
Laryngoscopy
MRI
Autopsy
Abundant secretions Posterior lingual fall Base of tongue congestion Adduction of vocal cords
5 2 [3,5] 2 [1,4] 5
0 2 [3,5] 2 [1,4] 5
0 0 2 [1,4] 0
S. Duband et al. / Forensic Science International 192 (2009) 48–52
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Fig. 1. (A) Microscopic appearances of hemorrhage surrounding jugular and carotid vessels (HES, 100, JV = internal jugular vein, C = carotid artery, VN = vagal nerve); (B) fracture of the hyoid bone (up: macroscopic aspect, down: histological section, HES, 100); (C) emphysema aspect of lung (HES, 100).
Fig. 2. (A) Sagittal T2-weighted MRI aspect of tongue congestion (hyperintense signal) and posterior fall with complete obstruction of airway (white arrow); (B) microscopic appearance of lingual congestion (HES, 100).
3.4. Comparison of endolaryngeal findings on laryngoscopy in hanging and non-hanging cases The laryngoscopy findings in hanging and non-hanging cases are shown in Table 4. Table 4 Laryngeal findings in hanging and non-hanging cases (the sixth observation was taken account for hanging group). Laryngoscopy findings
Hanging cases (N = 6)
Non-hanging cases (N = 3)
Abundant secretions Posterior lingual fall Base of tongue congestion Adduction of vocal cords
6 2 [3,5] 2 [1,4] 6
1 [7] 1 [7] 0 0
The secretions found in the larynx of the seventh observation contained some food fragments due to gastric regurgitation inhalation. The vocal cords of the non-hanging cases were in the intermediate position (between adduction and abduction, Fig. 4) maintaining an aperture of the larynx. 3.5. Evolution in time of endolaryngeal findings on laryngoscopy in a hanging case Because of possible modification in time of the laryngeal configuration due to postmortem changes, we performed two successive laryngoscopy examinations at 48-h intervals in case no. 6, for whom no autopsy was required. The first was performed 24 h after death. Any modification of laryngeal configuration between
S. Duband et al. / Forensic Science International 192 (2009) 48–52
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Fig. 3. (A) Endoscopic aspect of vocal cord adduction in hanging case (the dotted line indicates the middle line; E = epiglottis, LVC = left vocal cord, AC = arytenoid cartilage); (B) the same aspect in axial T1-weighted MR image (white arrow shows the anterior commissure).
tomography for optimum bone and cartilage examination. In one case of complete typical hanging (case no. 3), we observed cervical perispinal bleeding with cervical spine ligament distention without rupture or medullar injury previously described by Reay et al. [9]. Laryngeal secretions were not observed with MRI because they were aspired before, during the laryngofibroscopy. The obstruction of the upper airway by the posterior placement of the root of the tongue is difficult to attribute to an ante-mortem change. This position could be explained by the traction of the noose forcing back the tongue and pressing it against the posterior wall of the pharynx as it was already described. 4.2. Cadaveric position of vocal cords and vocal cord position in hanging cases
Fig. 4. Endoscopic aspect of vocal cords in a non-hanging case of death (the dotted line simulates the middle line; E = epiglottis, LVC = left vocal cord, RAC = right arytenoid cartilage).
these two laryngoscopies was observed. The vocal cords at 24 and 72 h after death were in the adduction position with contact in the median plane. 4. Discussion 4.1. Comparison of imaging and autopsy findings in hanging cases Literature data on MRI findings in hanging cases mainly relate to ‘‘spectacular’’ injuries to the brain or neck and lacking when it comes to the classical signs observed in usual cases [5–7]. Yen et al. [7] have described some MRI findings in five hanging cases and our results are very similar to this article. However, unlike these authors, we have never observed lymph node and salivary gland hemorrhages. These two findings could relate to the type of hanging (complete and incomplete) or to the cervical position of link and knot not related in this work. As shown by the forensic team of Bern, MRI does not allow for the detection of hyoid bone fracture and should be completed by a multislice spiral computed
The position of the vocal cords described in fresh cadavers (socalled cadaveric position of vocal cords) is an intermediate position between adduction and abduction, slightly lateral to midline [10], as observed in our non-hanging cases. However, this position has never been correlated with postmortem delay and was obtained on dissected larynges. Vocal cord configuration may vary in time according to installation and resolution of rigor mortis. However, to our knowledge, data concerning rigor mortis evolution in the laryngeal muscles are not available in the international literature. We can observe that for approximately the same postmortem delay between hanging and non-hanging cases, the vocal cords were not found in the same position. In the hanging cases, the vocal cord position differed from the usually described cadaveric position. In fact, the vocal cords were against one another, completely blocking the upper airway. In clinical practice, this position is also observed in bilateral vocal cord paralysis in adduction known as Riegel and Gerhardt syndromes [11] or during laryngospasm, leading to vocal dysfunction and acute dyspnea. The two successive laryngoscopy examinations at 24 and 72 h of death in case no. 6 suggest that this postmortem position in adduction is maintained 72 h after death in our conditions of preservation. In all cases, the period during which we performed the vocal cord observation coincides with the postmortem period when cadaveric stiffness is already set in as mentioned in Table 1. So, after death the laryngeal muscles become rigid and fixed in the position they were in the early postmortem interval. A persistent compression of the neck after death with an adjacent position of the vocal cords until onset of rigor mortis could not be excluded to
52
S. Duband et al. / Forensic Science International 192 (2009) 48–52
explain in some cases the closure of the glottis. But, the difference of vocal fold position between hanging and non-hanging cases could express behavioral difference before death in the two situations and then the glottis closure could vouch for a vital laryngeal spasm. The laryngeal spasm could be due to forces applied to the cervical nervous structures by ligature. This hypothesis could be supported by physiological studies and clinical practice:
4.4. Advantages and inconveniences of laryngoscopy examination in victims of hanging
Laryngospasm involves a complex system of nerves, all issued from the vagus nerve with a predominant cholinergic constrictor pathway [12,13]. Furthermore, a vagal response (reflex) is obtained after cervical stimulation of mechanoreceptors contained in the carotid glomi. In addition, the connections between laryngeal innervation and the vagal autonomic system are equally supported by a vagal response to laryngeal stimuli such as aspirations in the upper airway [14]. Also, the stimulation or inhibition of the high cervical portion of vagal nerves by prolonged compression of the neck could probably explain an active glottic closure. Moreover, animal experiments conducted on cats by Dixon et al. [15] and on dogs by Gonzalez-Baron et al. [16] showed that, after vagotomy, a laryngeal constriction appeared under asphyxial conditions. In another way, a major explanation could also be given. In fact, laryngospasm has recently been described as a possible cause of death in epilepsy [17]. Convulsions due to asphyxia are now a well known phenomenon attributed to cerebral anoxia and have been described during death by hanging [18]. So, laryngospasm could represent a major manifestation of cerebral hypoperfusion.
5. Conclusion
4.3. Arguments in considering the adduction of vocal cords as a vital sign of hanging The histological aspect of pulmonary parenchyma usually observed in death by hanging consists in emphysema with alveolar hemorrhagic edema [19,20]. This feature is characteristic of an increase in intrapulmonary pressure. Now, since the Brouardel experiments, it is accepted that in hangings, notably incomplete, forces applied to the neck are not sufficient to crush the laryngeal structures or to close the rima glottidis [21,22]. Furthermore in all of our six hanging cases, the cervical compression is above the thyroid cartilage prominence and consequently above the glottic plane. Therefore, the microscopic appearance of lungs in hanging could not only be attributed to crushing of the larynx by neck ligature. This aspect could, however, result from an increase in thoracic pressure provoked by expiration movements against a closed glottis. In addition, larynx innervation is insured by the superior and inferior (recurrent) laryngeal nerves, two branches of the vagus nerves, which have a deep cervical position next to the jugular and carotid vessels. These vascular structures are compressed by cervical ligature during hanging and this crushing is responsible for cerebral anoxia. Consequently, if the cervical great vessels are compressed, vagal compression seems to leave no doubt. Finally, the stagnation of abundant secretions on the upper side of the vocal cords noticed during the laryngoscopy is also an important argument for vital ante-mortem glottis closure. Furthermore, this abundance could be a sign of vegetative hyperstimulation of the secretion during hanging. The involvement of the vegetative nervous system is also supposed to explain a reflex cardiac arrest in cervical ligature cases [23,24]. Thus a laryngeal closure reflex by vocal fold adduction (i.e. laryngospasm) due to cervical compression during hanging could explain a real asphyxial mechanism even if the suspension was partial and not enough to crush the upper airway.
The laryngofibroscopy technique is easy to implement in a forensic department by using portable equipment. However, rigor mortis makes mobilization of the head and neck of cadavers very difficult, which could limit the angles of sight of certain pharyngeal and laryngeal regions.
Further studies are naturally indispensable in order to confirm our observations and to understand the traumatic mechanisms involved in hanging cases. Nevertheless, laryngofibroscopy examination appears to be a very useful tool to complete the autopsy procedure in hanging investigations. In addition, new imaging methods are valuable in forensic medicine, on one hand, to refine thanatologic semiology and, on the other hand, to improve the physiopathological knowledge of deaths. References [1] J. Simonsen, Patho-anatomic findings in neck structures in asphyxiation due to hanging. A survey of 80 cases, Forensic Sci. Int. 38 (1988) 83–91. [2] R. James, P. Silcoks, Suicidal hanging in Cardiff: a 15-years retrospective study, Forensic Sci. Int. 56 (1992) 167–175. [3] I. Morild, Fractures of neck structures in suicidal hanging, Med. Sci. Law 36 (1996) 80–84. [4] V.D. Khokhlov, Injuries to the hyoid bone and laryngeal cartilages: effectiveness of different methods of medico-legal investigation, Forensic Sci. Int. 88 (1997) 173– 183. [5] S.K. Wallace, W.A. Cohen, E.J. Stern, D.T. Reay, Judicial hanging: postmortem radiographic, CT, and MR Imaging features with autopsy confirmation, Radiology 193 (1994) 263–267. [6] M.J. Thali, K. Yen, W. Schweitzer, P. Vock, C. Boesch, C. Ozdoba, G. Schroth, M. Ith, M. Sonnenschein, T. Doernhoefer, E. Scheurer, T. Plattner, R. Dirnhofer, Virtopsy, a new imaging horizon in forensic pathology: virtual autopsy by postmortem multislice computed tomography (MSCT) and magnetic resonance imaging (MRI)—a feasibility study, J. Forensic Sci. 48 (2003) 386–403. [7] K. Yen, M.J. Thali, E. Aghayev, C. Jackowski, W. Schweitzer, C. Boesch, P. Vock, R. Dirnhofer, M. Sonnenschein, Strangulation signs: Initial correlation of MRI, MSCT, and forensic neck findings, J. Magn. Reson. Imaging 22 (2005) 501–510. [8] I. Prinsloo, I. Gordon, Post-mortem dissection artefacts of the neck: their differentiation from ante-mortem bruises, SA Med. J. 25 (1951) 358–361. [9] D.T. Reay, W. Cohen, S. Ames, Injuries produced by judicial hanging. A case report, Am. J. Forensic Med. Pathol. 15 (1994) 183–186. [10] R.J. England, A.D. Wilde, J.C. McIlwain, The posterior cricoarythenoid ligaments and their relationship to the cadaveric position of the vocal cords, Clin. Otolaryngol. Allied Sci. 21 (1996) 425–428. [11] B.T. King, R.L. Gregg, An anatomical reason for the various behaviors of paralyzed vocal cords, Ann. Otol. Rhinol. Laryngol. 57 (1948) 925–944. [12] J. Widdicombe, Control of airway caliber, Am. Rev. Respir. Dis. 131 (1985) S33–S35. [13] C.L. Ludlow, Central nervous system control of the laryngeal muscles in humans, Respir. Physiol. Neurobiol. 147 (2005) 205–222. [14] E.T. Cunningham Jr., W.J. Ravich, B. Jones, M.W. Donner, Vagal reflexes referred from the upper aerodigestive tract: an infrequently recognized cause of common cardiorespiratory responses, Ann. Intern. Med. 116 (1992) 575–582. [15] M. Dixon, J.G. Widdicombe, J.C.M. Wise, Studies on laryngeal calibre during stimulation of peripheral and central chemoreceptors, pneumothorax and increased respiratory loads, J. Physiol. 239 (1974) 347–363. [16] S. Gonza´lez-Baro´n, M. Molina, F. Garcı´a Matilla, A. Bogas, Vagal control of larynx resistance to the air flow, Rev. Esp. Fisiol. 35 (1979) 291–306. [17] J. Tavee, H. Morris 3rd., Severe postictal laryngospasm as a potential mechanism for sudden unexpected death in epilepsy: a near-miss in an EMU, Epilepsia (2008) [Epub ahead of print]. [18] A. Sauvageau, S. Racette, Agonal sequences in a filmed suicidal hanging: analysis of respiratory and movement responses to asphyxia by hanging, J. Forensic Sci. 52 (2007) 957–959. [19] W. Grellner, B. Madea, Pulmonary micromorphology in fatal strangulations, Forensic Sci. Int. 67 (1994) 109–125. [20] M.J. Shkrum, D.A. Ramsay, Forensic Pathology of Trauma, Common Problems for the Pathologist, Humana Press, New Jersey, 2007. [21] P. Brouardel, La Pendaison, La Strangulation, La Suffocation, La Submersion, IB Bailliere et fils, Paris, 1897. [22] V.D. Khokhlov, Calculation of tension exerted on a ligature in incomplete hanging, Forensic Sci. Int. 123 (2001) 172–177. [23] B. Knight, P. Saukko, Knight’s Forensic Pathology, 3rd ed., Arnold, London, 2004. [24] V.J.M. Di Maio, D Di Maio, Forensic Pathology, 2nd ed., CRC Press, New York, 2001.
Contents lists available at ScienceDirect
Forensic Science International journal homepage: www.elsevier.com/locate/forsciint
Study of endolaryngeal structures by videolaryngoscopy after hanging: A new approach to understanding the physiopathogenesis S. Duband a,b,*, A.P. Timoshenko c,d, R. Mohammedi e, J.-M. Prades c,d, F.-G. Barral e, M. Debout a, M. Pe´oc’h a,b,1 a
Department of Forensic Medicine, Saint-Etienne University Hospital Center, Bellevue Hospital, 42055 St-Etienne, Cedex 2, France Department of Pathology, Saint-Etienne University Hospital Center, North Hospital, 42055 St-Etienne, Cedex 2, France Department of Otolaryngology-Head and Neck Surgery, Saint-Etienne University Hospital Center, North Hospital, 42055 St-Etienne, Cedex 2, France d Department of Anatomy, Jacques Lisfranc Faculty of Medicine, Jean Monnet University, 15 rue Ambroise Pare´, 42023 St-Etienne, Cedex 2, France e Department of Radiology, Saint-Etienne University Hospital Center, Bellevue Hospital, 42055 St-Etienne, Cedex 2, France b c
A R T I C L E I N F O
A B S T R A C T
Article history: Received 20 October 2008 Received in revised form 16 July 2009 Accepted 21 July 2009 Available online 20 August 2009
Purpose: To evaluate laryngoscopic findings in hanging cases and to compare them with magnetic resonance imaging (MRI) and forensic autopsy results. Materials and methods: Postmortem nasolaryngofibroscopy and MRI of five people who died from hanging were performed. Three people who died from other causes than hanging were also examined with a flexible laryngofibroscope. The results were compared with injuries discovered during forensic autopsy. Results: In all five hanging cases, laryngofibroscopic investigation showed a vocal fold position in complete adduction confirmed by MRI. This position did not seem to be influenced by the intensity of the forces applied to neck or postmortem delay and cadaveric phenomena. The vocal cords of the three nonhanging deceased were found in the intermediate position. These findings could suggest that pressure applied to the cervical nervous and cartilaginous structures or their elongation during hanging could lead to closure of the glottis with vocal cord adduction maintained after death. Conclusion: Laryngofibroscopic examination in hanging cases could be very useful in confirming the vital character of the hanging and understanding asphyxial phenomena in incomplete suspension without laryngeal crush. ß 2009 Elsevier Ireland Ltd. All rights reserved.
Keywords: Hanging Nasolaryngofibroscopy Larynx Vocal cords Vocal cords position Forensic interest
1. Introduction Because there is no pathognomonic sign of hanging, its diagnosis is difficult to categorically establish and is always based on several arguments but can sometimes be uncertain if vital injuries are absent or invisible. Although in current forensic practice, such injuries as soft-tissue cervical hemorrhages or vital fractures of laryngeal skeleton are systematically researched and regularly published [1– 3], the appearance of the endolarynx is never highlighted. Furthermore, the diagnosis of vital signs depends on the techniques used [4]. Several authors currently affirm that multislice spiral computed tomography (MSCT) and magnetic resonance imaging (MRI) offer great potential for the detection of these injuries [5–7]. In the following, magnetic resonance imaging, videolaryngo-
* Corresponding author at: Department of Forensic Medicine, University Hospital Center of Saint-Etienne, 42055 Saint-Etienne, Cedex 2, France. Tel.: +33 (0)4 77 12 05 23; fax: +33 (0)4 77 12 09 16. E-mail address: [email protected] (S. Duband). 1 Tel.: +33 (0)4 77 12 05 23; fax: +33 (0)4 77 12 09 16. 0379-0738/$ – see front matter ß 2009 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.forsciint.2009.07.015
fibroscopy and autopsy findings of five asphyxia fatalities by hanging are analyzed and compared with three non-hanging deceased. The aim of this study was to evaluate the appearance of the endolarynx and the benefit of laryngofibroscopic examination as possible diagnostic tools of hanging in postmortem situations. 2. Materials and methods 2.1. Subjects The responsible justice department approved the present study. Five cases of suicidal hanging described in Table 1 (five males, mean age = 51 years, age range = 33–83) were examined using postmortem pre-autopsy MRI and videolaryngofibroscopy. One case (case 6, male, 25 years), for which autopsy was not required, was only investigated by two successive laryngofibroscopy examinations at 48-h intervals. Three non-hanging deceased (cases 7–9, males, mean age = 54 years) were only investigated by laryngofibroscopy within 24 and 48 h after death (no data being available in the literature) for comparison. All of the corpses were undressed and examined externally prior to scanning and autopsy by a forensic pathologist. The body mass index (BMI), the type of hanging and the link used were recorded. The time since death was evaluated using current standard methods of body temperature, degree of rigor mortis and investigation data. The time of suspension was approximated from the time since death and police and detailed interviews of the relatives of the deceased. The results of the external examination were recorded, e.g. conjunctival congestion or bleeding, cyanosis, visible neck
S. Duband et al. / Forensic Science International 192 (2009) 48–52
49
Table 1 Characteristics of subjects and hangings of study. Case
Age (years)
BMI
Link
Type of hanging
1
48
22.9
Rope
2
33
23.7
Girths
3
33
22.3
4
83
28.4
Electric extension Rope
5
58
23.4
Girths
6
25
19.9
Rope
7 8 9
29 59 75
20.8 26.3 23.2
– – –
Atypical incomplete Atypical incomplete Typical complete Atypical unknown Atypical incomplete Atypical complete – – –
Characteristics of cervical compression
Suspension time (h)
Type of knot
Anatomical position of loop
Anatomical position of knot
Slip knot
Above thyroid prominence Above thyroid prominence Above thyroid prominence Above thyroid prominence Above thyroid prominence Above thyroid prominence – – –
cartilage
Regarding left mastoid
41
cartilage
Regarding left mastoid
12 2
cartilage
No visible print
cartilage
Behind left mandibular angle
cartilage
No visible print
81
cartilage
No visible print
51
– – –
– – –
Slip knot Fixed knot Slip knot Fixed knot Fixed knot – – –
injuries, etc. The bodies were preserved at a temperature of 4 8C after their admission to the forensic department and prior to the different examinations. 2.2. Postmortem MRI and videolaryngofibroscopy The telelaryngoscopy examinations were conducted using a flexible nasolaryngofibroscope Olympus ENF type P4 and conventional video system with microcamera Storz tricam. Images were digitalized using image capturing program E-capture (Metris). For MRI, the bodies were wrapped in artifact-free body bags to prevent contamination of materials. All MR examinations were performed with a 1.5-T system (Intera Achieva 1.5 T; Phillips) and consisted in T1, T2 fast spin-echo (FSE) and short-tau inversion recovery (STIR) sequences with an antneck coil (Neurovascular 8 channel Array head-neck). The mean times between estimated death, laryngofibroscopy examination and imaging were 27 and 38 h, respectively. 2.3. Forensic autopsy A standard autopsy was performed according to current guidelines at an average time of 9 h after imaging. The layer by layer neck dissection was undertaken after evisceration of the other organs following the protocol of Prinsloo and Gordon [8] and the cervical spine was extracted and examined after removal of vertebral body. In all the autopsied cases, samples of each major organ and injured tissue were histologically analyzed after formalin fixation, embedding in paraffin and hematoxylin–eosin–saffron staining. After macroscopic examination, when a fracture was present, the laryngeal skeleton conserving the surrounding adherent soft tissue was decalcified with a 10% HNO3 solution and microscopically examined. 2.4. Data analysis A direct comparison of the imaging, videolaryngofibroscopy, autopsy and histology findings was carried out taking the autopsy and histology data as reference.
3. Results 3.1. Subject and hanging characteristics The main subject and hanging characteristics are summarized in Table 1. In all the hanging cases, the ligature mark on the neck was always above the thyroid cartilage prominence. The causes of death revealed by autopsy and toxicological analysis of blood, urine and gastric content samples of the last three subjects (cases 7–9) were opioid intoxication, myocardial infarct and ballistic intracranial trauma, respectively. 3.2. Comparison of autopsy and imaging findings in hanging cases The results of comparison between autopsy and imaging findings concerning neck structures except for buccal and endolaryngeal elements are shown in Table 2.
71 43 4
Table 2 Cervical findings by MRI and autopsy (N = 5, and the number of the observations is indicated in brackets). Findings
MRI
Autopsy
Subcutaneous hemorrhage Intramuscular hemorrhage Perivascular hemorrhage Fracture of hyoid bone Fracture of laryngeal cartilages Sinusal lymph node congestion Epidural cervical spinal hemorrhage
3 4 1 0 0 3 1
4 4 1 1 0 3 1
[1,3,4] [1,3–5] [4]
[2,3,5] [3]
[1,3–5] [1,3–5] [4]; Fig. 1A [2]; Fig. 1B [2,3,5] [3]
In all cases, the autopsy suggested the asphyxial nature of death and the histological aspect of the lungs were similar and consisted in emphysema (Fig. 1C). In these five observations, hanging was due to suicide attempt. 3.3. Comparison of buccal and endolaryngeal findings on autopsy, laryngoscopy and imaging in hanging cases The results of correlation of laryngofibroscopy, MRI and autopsy findings concerning the endobuccal and endolaryngeal structures are summarized in Table 3. The abundance of secretions found during nasolaryngofibroscopy (performed in all cases before MRI) above the glottic plane required an aspiration system to progress into the laryngeal tract. The posterior placement of the root of the tongue observed in two cases was responsible for complete obstruction of the oropharynx in the median plane (Fig. 2A). The base of tongue congestion (Fig. 2B) gave a cyanic pseudo-ecchymotic aspect to this anatomical region with laryngoscopic examination and hypersignal in T2-weighted MRI. In all cases, vocal cord adduction in the median plane was observed with contact between the vocal processes of arytenoid cartilages (Fig. 3).
Table 3 Endolaryngeal findings at laryngoscopy and imaging examinations and autopsy (N = 5). Findings
Laryngoscopy
MRI
Autopsy
Abundant secretions Posterior lingual fall Base of tongue congestion Adduction of vocal cords
5 2 [3,5] 2 [1,4] 5
0 2 [3,5] 2 [1,4] 5
0 0 2 [1,4] 0
S. Duband et al. / Forensic Science International 192 (2009) 48–52
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Fig. 1. (A) Microscopic appearances of hemorrhage surrounding jugular and carotid vessels (HES, 100, JV = internal jugular vein, C = carotid artery, VN = vagal nerve); (B) fracture of the hyoid bone (up: macroscopic aspect, down: histological section, HES, 100); (C) emphysema aspect of lung (HES, 100).
Fig. 2. (A) Sagittal T2-weighted MRI aspect of tongue congestion (hyperintense signal) and posterior fall with complete obstruction of airway (white arrow); (B) microscopic appearance of lingual congestion (HES, 100).
3.4. Comparison of endolaryngeal findings on laryngoscopy in hanging and non-hanging cases The laryngoscopy findings in hanging and non-hanging cases are shown in Table 4. Table 4 Laryngeal findings in hanging and non-hanging cases (the sixth observation was taken account for hanging group). Laryngoscopy findings
Hanging cases (N = 6)
Non-hanging cases (N = 3)
Abundant secretions Posterior lingual fall Base of tongue congestion Adduction of vocal cords
6 2 [3,5] 2 [1,4] 6
1 [7] 1 [7] 0 0
The secretions found in the larynx of the seventh observation contained some food fragments due to gastric regurgitation inhalation. The vocal cords of the non-hanging cases were in the intermediate position (between adduction and abduction, Fig. 4) maintaining an aperture of the larynx. 3.5. Evolution in time of endolaryngeal findings on laryngoscopy in a hanging case Because of possible modification in time of the laryngeal configuration due to postmortem changes, we performed two successive laryngoscopy examinations at 48-h intervals in case no. 6, for whom no autopsy was required. The first was performed 24 h after death. Any modification of laryngeal configuration between
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Fig. 3. (A) Endoscopic aspect of vocal cord adduction in hanging case (the dotted line indicates the middle line; E = epiglottis, LVC = left vocal cord, AC = arytenoid cartilage); (B) the same aspect in axial T1-weighted MR image (white arrow shows the anterior commissure).
tomography for optimum bone and cartilage examination. In one case of complete typical hanging (case no. 3), we observed cervical perispinal bleeding with cervical spine ligament distention without rupture or medullar injury previously described by Reay et al. [9]. Laryngeal secretions were not observed with MRI because they were aspired before, during the laryngofibroscopy. The obstruction of the upper airway by the posterior placement of the root of the tongue is difficult to attribute to an ante-mortem change. This position could be explained by the traction of the noose forcing back the tongue and pressing it against the posterior wall of the pharynx as it was already described. 4.2. Cadaveric position of vocal cords and vocal cord position in hanging cases
Fig. 4. Endoscopic aspect of vocal cords in a non-hanging case of death (the dotted line simulates the middle line; E = epiglottis, LVC = left vocal cord, RAC = right arytenoid cartilage).
these two laryngoscopies was observed. The vocal cords at 24 and 72 h after death were in the adduction position with contact in the median plane. 4. Discussion 4.1. Comparison of imaging and autopsy findings in hanging cases Literature data on MRI findings in hanging cases mainly relate to ‘‘spectacular’’ injuries to the brain or neck and lacking when it comes to the classical signs observed in usual cases [5–7]. Yen et al. [7] have described some MRI findings in five hanging cases and our results are very similar to this article. However, unlike these authors, we have never observed lymph node and salivary gland hemorrhages. These two findings could relate to the type of hanging (complete and incomplete) or to the cervical position of link and knot not related in this work. As shown by the forensic team of Bern, MRI does not allow for the detection of hyoid bone fracture and should be completed by a multislice spiral computed
The position of the vocal cords described in fresh cadavers (socalled cadaveric position of vocal cords) is an intermediate position between adduction and abduction, slightly lateral to midline [10], as observed in our non-hanging cases. However, this position has never been correlated with postmortem delay and was obtained on dissected larynges. Vocal cord configuration may vary in time according to installation and resolution of rigor mortis. However, to our knowledge, data concerning rigor mortis evolution in the laryngeal muscles are not available in the international literature. We can observe that for approximately the same postmortem delay between hanging and non-hanging cases, the vocal cords were not found in the same position. In the hanging cases, the vocal cord position differed from the usually described cadaveric position. In fact, the vocal cords were against one another, completely blocking the upper airway. In clinical practice, this position is also observed in bilateral vocal cord paralysis in adduction known as Riegel and Gerhardt syndromes [11] or during laryngospasm, leading to vocal dysfunction and acute dyspnea. The two successive laryngoscopy examinations at 24 and 72 h of death in case no. 6 suggest that this postmortem position in adduction is maintained 72 h after death in our conditions of preservation. In all cases, the period during which we performed the vocal cord observation coincides with the postmortem period when cadaveric stiffness is already set in as mentioned in Table 1. So, after death the laryngeal muscles become rigid and fixed in the position they were in the early postmortem interval. A persistent compression of the neck after death with an adjacent position of the vocal cords until onset of rigor mortis could not be excluded to
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explain in some cases the closure of the glottis. But, the difference of vocal fold position between hanging and non-hanging cases could express behavioral difference before death in the two situations and then the glottis closure could vouch for a vital laryngeal spasm. The laryngeal spasm could be due to forces applied to the cervical nervous structures by ligature. This hypothesis could be supported by physiological studies and clinical practice:
4.4. Advantages and inconveniences of laryngoscopy examination in victims of hanging
Laryngospasm involves a complex system of nerves, all issued from the vagus nerve with a predominant cholinergic constrictor pathway [12,13]. Furthermore, a vagal response (reflex) is obtained after cervical stimulation of mechanoreceptors contained in the carotid glomi. In addition, the connections between laryngeal innervation and the vagal autonomic system are equally supported by a vagal response to laryngeal stimuli such as aspirations in the upper airway [14]. Also, the stimulation or inhibition of the high cervical portion of vagal nerves by prolonged compression of the neck could probably explain an active glottic closure. Moreover, animal experiments conducted on cats by Dixon et al. [15] and on dogs by Gonzalez-Baron et al. [16] showed that, after vagotomy, a laryngeal constriction appeared under asphyxial conditions. In another way, a major explanation could also be given. In fact, laryngospasm has recently been described as a possible cause of death in epilepsy [17]. Convulsions due to asphyxia are now a well known phenomenon attributed to cerebral anoxia and have been described during death by hanging [18]. So, laryngospasm could represent a major manifestation of cerebral hypoperfusion.
5. Conclusion
4.3. Arguments in considering the adduction of vocal cords as a vital sign of hanging The histological aspect of pulmonary parenchyma usually observed in death by hanging consists in emphysema with alveolar hemorrhagic edema [19,20]. This feature is characteristic of an increase in intrapulmonary pressure. Now, since the Brouardel experiments, it is accepted that in hangings, notably incomplete, forces applied to the neck are not sufficient to crush the laryngeal structures or to close the rima glottidis [21,22]. Furthermore in all of our six hanging cases, the cervical compression is above the thyroid cartilage prominence and consequently above the glottic plane. Therefore, the microscopic appearance of lungs in hanging could not only be attributed to crushing of the larynx by neck ligature. This aspect could, however, result from an increase in thoracic pressure provoked by expiration movements against a closed glottis. In addition, larynx innervation is insured by the superior and inferior (recurrent) laryngeal nerves, two branches of the vagus nerves, which have a deep cervical position next to the jugular and carotid vessels. These vascular structures are compressed by cervical ligature during hanging and this crushing is responsible for cerebral anoxia. Consequently, if the cervical great vessels are compressed, vagal compression seems to leave no doubt. Finally, the stagnation of abundant secretions on the upper side of the vocal cords noticed during the laryngoscopy is also an important argument for vital ante-mortem glottis closure. Furthermore, this abundance could be a sign of vegetative hyperstimulation of the secretion during hanging. The involvement of the vegetative nervous system is also supposed to explain a reflex cardiac arrest in cervical ligature cases [23,24]. Thus a laryngeal closure reflex by vocal fold adduction (i.e. laryngospasm) due to cervical compression during hanging could explain a real asphyxial mechanism even if the suspension was partial and not enough to crush the upper airway.
The laryngofibroscopy technique is easy to implement in a forensic department by using portable equipment. However, rigor mortis makes mobilization of the head and neck of cadavers very difficult, which could limit the angles of sight of certain pharyngeal and laryngeal regions.
Further studies are naturally indispensable in order to confirm our observations and to understand the traumatic mechanisms involved in hanging cases. Nevertheless, laryngofibroscopy examination appears to be a very useful tool to complete the autopsy procedure in hanging investigations. In addition, new imaging methods are valuable in forensic medicine, on one hand, to refine thanatologic semiology and, on the other hand, to improve the physiopathological knowledge of deaths. References [1] J. Simonsen, Patho-anatomic findings in neck structures in asphyxiation due to hanging. A survey of 80 cases, Forensic Sci. Int. 38 (1988) 83–91. [2] R. James, P. Silcoks, Suicidal hanging in Cardiff: a 15-years retrospective study, Forensic Sci. Int. 56 (1992) 167–175. [3] I. Morild, Fractures of neck structures in suicidal hanging, Med. Sci. Law 36 (1996) 80–84. [4] V.D. Khokhlov, Injuries to the hyoid bone and laryngeal cartilages: effectiveness of different methods of medico-legal investigation, Forensic Sci. Int. 88 (1997) 173– 183. [5] S.K. Wallace, W.A. Cohen, E.J. Stern, D.T. Reay, Judicial hanging: postmortem radiographic, CT, and MR Imaging features with autopsy confirmation, Radiology 193 (1994) 263–267. [6] M.J. Thali, K. Yen, W. Schweitzer, P. Vock, C. Boesch, C. Ozdoba, G. Schroth, M. Ith, M. Sonnenschein, T. Doernhoefer, E. Scheurer, T. Plattner, R. Dirnhofer, Virtopsy, a new imaging horizon in forensic pathology: virtual autopsy by postmortem multislice computed tomography (MSCT) and magnetic resonance imaging (MRI)—a feasibility study, J. Forensic Sci. 48 (2003) 386–403. [7] K. Yen, M.J. Thali, E. Aghayev, C. Jackowski, W. Schweitzer, C. Boesch, P. Vock, R. Dirnhofer, M. Sonnenschein, Strangulation signs: Initial correlation of MRI, MSCT, and forensic neck findings, J. Magn. Reson. Imaging 22 (2005) 501–510. [8] I. Prinsloo, I. Gordon, Post-mortem dissection artefacts of the neck: their differentiation from ante-mortem bruises, SA Med. J. 25 (1951) 358–361. [9] D.T. Reay, W. Cohen, S. Ames, Injuries produced by judicial hanging. A case report, Am. J. Forensic Med. Pathol. 15 (1994) 183–186. [10] R.J. England, A.D. Wilde, J.C. McIlwain, The posterior cricoarythenoid ligaments and their relationship to the cadaveric position of the vocal cords, Clin. Otolaryngol. Allied Sci. 21 (1996) 425–428. [11] B.T. King, R.L. Gregg, An anatomical reason for the various behaviors of paralyzed vocal cords, Ann. Otol. Rhinol. Laryngol. 57 (1948) 925–944. [12] J. Widdicombe, Control of airway caliber, Am. Rev. Respir. Dis. 131 (1985) S33–S35. [13] C.L. Ludlow, Central nervous system control of the laryngeal muscles in humans, Respir. Physiol. Neurobiol. 147 (2005) 205–222. [14] E.T. Cunningham Jr., W.J. Ravich, B. Jones, M.W. Donner, Vagal reflexes referred from the upper aerodigestive tract: an infrequently recognized cause of common cardiorespiratory responses, Ann. Intern. Med. 116 (1992) 575–582. [15] M. Dixon, J.G. Widdicombe, J.C.M. Wise, Studies on laryngeal calibre during stimulation of peripheral and central chemoreceptors, pneumothorax and increased respiratory loads, J. Physiol. 239 (1974) 347–363. [16] S. Gonza´lez-Baro´n, M. Molina, F. Garcı´a Matilla, A. Bogas, Vagal control of larynx resistance to the air flow, Rev. Esp. Fisiol. 35 (1979) 291–306. [17] J. Tavee, H. Morris 3rd., Severe postictal laryngospasm as a potential mechanism for sudden unexpected death in epilepsy: a near-miss in an EMU, Epilepsia (2008) [Epub ahead of print]. [18] A. Sauvageau, S. Racette, Agonal sequences in a filmed suicidal hanging: analysis of respiratory and movement responses to asphyxia by hanging, J. Forensic Sci. 52 (2007) 957–959. [19] W. Grellner, B. Madea, Pulmonary micromorphology in fatal strangulations, Forensic Sci. Int. 67 (1994) 109–125. [20] M.J. Shkrum, D.A. Ramsay, Forensic Pathology of Trauma, Common Problems for the Pathologist, Humana Press, New Jersey, 2007. [21] P. Brouardel, La Pendaison, La Strangulation, La Suffocation, La Submersion, IB Bailliere et fils, Paris, 1897. [22] V.D. Khokhlov, Calculation of tension exerted on a ligature in incomplete hanging, Forensic Sci. Int. 123 (2001) 172–177. [23] B. Knight, P. Saukko, Knight’s Forensic Pathology, 3rd ed., Arnold, London, 2004. [24] V.J.M. Di Maio, D Di Maio, Forensic Pathology, 2nd ed., CRC Press, New York, 2001.