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Positional asphyxia or diabetic ketoacidosis? A case report
Legal Medicine 13 (2011) 196–200
Contents lists available at ScienceDirect
Legal Medicine journal homepage: www.elsevier.com/locate/legalmed
Case Report
Positional asphyxia or diabetic ketoacidosis? A case report Takahito Hayashi ⇑, Kazutoshi Ago, Mihoko Ago, Mamoru Ogata Department of Legal Medicine, Graduate School of Medical and Dental Sciences, Kagoshima University, 8-35-1 Sakuragaoka, Kagoshima 890-8544, Japan
a r t i c l e
i n f o
Article history: Received 25 December 2010 Received in revised form 27 January 2011 Accepted 31 January 2011 Available online 4 March 2011 Keywords: Diabetic ketoacidosis (DKA) Head-down position Positional asphyxia Diabetes mellitus Forensic pathology Cause of death
a b s t r a c t We describe an autopsy case in which a patient with diabetic ketoacidosis (DKA) was found in a headdown position. A female in her late 70s was found dead in her home in a supine position on the kitchen floor. The upper part of her body was hanging down over the edge of the kitchen floor to the backyard through the open window. External examination revealed congestion of the head and upper region of the face and neck. There were numerous petechiae on the superior palpebral conjunctivae and upper part of the oral mucosa. On internal examination, extensive hemorrhages in the subcutaneous fat tissues and muscles were observed at the upper part of the neck, although there were no external injuries on the neck. Histopathological examination revealed that hemorrhages were accompanied with infiltration of polymorphonuclear leukocytes both within and around the hemorrhages on the neck skin. Nodular glomerulosclerosis and many fat droplets in the cytoplasm of proximal tubule cells were found in the kidney. Postmortem blood analysis showed acetone (204.2 lg/ml), HbA1c (10.8%), acetoacetate (<2.0 lmol/ l), 3-hydroxybutyrate (11,844 lmol/l), blood urea nitrogen (128.9 mg/dl), and creatinine (3.11 mg/dl). The glucose and acetone levels in the urine were 876.7 mg/dl and 201.4 lg/ml, respectively, suggesting that she suffered severe DKA. However, since hemorrhage of the neck could have developed only when she was still alive, asphyxia should have arisen antemortem. Based on these findings, we concluded that the direct cause of her death is positional asphyxia, which was resulted from DKA. It is difficult to diagnose the cause of death when the victim is in an unusual posture. To confirm a suspicion of positional asphyxia, photographs of the undisturbed scene are useful in addition to a precise autopsy and accurate examinations. Ó 2011 Elsevier Ireland Ltd. All rights reserved.
1. Introduction An increased incidence of death in a head-down position has been reported [1–5]. Common features in these cases include (a) the body in an inverted or head-down tilted position, (b) marked congestion of the face, scalp, neck, and other dependent parts of the body (hands and shoulders), (c) accompanying effects of the internal congestion with swelling of and petechial bleedings at the affected parts, as well as edema of the brain and lungs, and (d) lack of a definite pathoanatomical cause of death [1]. Although the pathophysiology of death in a head-down position is not fully understood, several previous reports suggest that death results from asphyxia due to fixation of the chest with hindering of thoracic movements and ventilation, and/or by circulatory failure due to marked depletion of the venous return to the heart [2–4]. Asphyxia caused by the adoption of particular positions in relation to unusual body posture that mechanically interferes with pulmonary ventilation is called ‘‘positional (postural) asphyxia’’ [6– 10]. However, it is often difficult to diagnose the cause of death ⇑ Corresponding author. Tel.: +81 99 275 5313; fax: +81 99 275 5315. E-mail address: [email protected] (T. Hayashi). 1344-6223/$ - see front matter Ó 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.legalmed.2011.01.006
in such cases because they generally present with an aspecific pathoanatomical picture [5,6]. In this report, we describe a case of death in a head-down position in a patient with diabetic ketoacidosis (DKA), and discuss the cause of death and the relationship of the position of the body to the death. 2. Case report A female in her late 70s was found dead in her home, lying naked except for a shirtwaist in a supine position on the kitchen floor with the upper part of her body hanging out of the open window to the backyard (Fig. 1). She bent her back and the upper part of her body including the head, face, neck, chest and upper extremities was situated below the kitchen floor. The left and right hands reached to the ground which was approximately 70 cm lower than the kitchen floor, whereas the head was hanging down loosely. Although the right upper extremity was found in a garbage box on the backyard, she was not wedged in a confined space. The lumber region was just situated on the windowsill (the edge of kitchen floor), and the gluteal region and both lower extremities spread apart were positioned on the kitchen floor. Although some
T. Hayashi et al. / Legal Medicine 13 (2011) 196–200
Fig. 1. Deceased at the scene.
underclothes, toilet papers and vomitus lay scattered on the floor around her, there were no objects that fixed the lower part of her body on the floor. Her position was not fixed by any forces. However, it was supposed that the position was stable, since the sacral region that corresponded to center of gravity of her body was left being on the kitchen floor. She was seen alive 2 days before. Police investigations revealed that she was diagnosed with type 2 diabetes mellitus (DM) approximately 10 years prior to death, but that she did not follow the medical service. An autopsy was carried out at approximately 2.5 days after death. 2.1. Autopsy findings The deceased was 145.0 cm tall and weighed 40.0 kg. External examination revealed dark purple-red discoloration of the head, upper region of the face and neck (Fig. 2). Numerous petechiae were found particularly on the superior palpebral conjunctivae and upper part of the oral mucosa. There were small abrasions and bruises on the back, and the upper and lower extremities. Internal examination revealed extensive hemorrhage of subcutaneous tissues of the neck (Fig. 3), although no external injuries were found on the neck. Hemorrhages were also noted in the cervical muscles such as platysma, left digastric muscle, bilateral mylohyoid muscles, and bilateral cricothyroid muscles. Those
Fig. 2. Congestion of the upper region of the face.
197
Fig. 3. Internal examinations of the neck. Hemorrhages of subcutaneous tissues were observed.
hemorrhages in soft tissues were localized predominantly to the upper part of the neck. No fractures of the hyoid bone, thyroid or cricoid cartilage were observed. Spotty subfascial hemorrhages in the left and right pectoralis major and minor muscles were observed. The brain weighed 1,220 g, and moderate edema was noted. Neither cerebral contusion nor hemorrhage was observed. The heart weighed 340 g, and many subepicardial petechiae were seen. A large amount of dark-red fluid blood mixed with fat-like and soft coagulated blood, was retained in the heart. Slight atherosclerosis was found on the coronary arteries. The left and right lungs weighed 310 g and 390 g, respectively, and both showed congestion. In the left and right lobe of the thyroid gland, solid tumors (3.0 1.4 1.5 cm, 2.5 2.0 1.5 cm in size, respectively) were found. There was a sharply circumscribed solid tumor (3.5 2.8 2.8 cm in size) in the left wall of the uterus. There were no remarkable findings in other organs except for congestion.
2.2. Histopathological findings Extensive hemorrhages accompanied with relatively marked infiltration of polymorphonuclear leukocytes both within and around the hemorrhages were found in the subcutaneous tissue of the neck skin (Fig. 4). Masson–Gomori staining for collagen fibers did not detect metachromasia of the cutaneous and subcutaneous connective tissue of the neck. There was small patchy loss of cardiac muscle cells in the left and right ventricles. In the kidney, PAS (Periodic acid-Schiff) staining-positive nodules were found in
Fig. 4. Histopathological examination revealed subcutaneous hemorrhages accompanied with relatively marked infiltration of polymorphonuclear leukocytes both within and around the hemorrhages of left lateral cervical region (HE). Original magnification, 50.
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T. Hayashi et al. / Legal Medicine 13 (2011) 196–200 Table 1 Data obtained from the postmortem physiochemical examination. Material Blood Serum Serum Serum Serum Serum Serum Serum Blood Urine Urine
Hemoglobin A1c Blood urea nitrogen Creatinine Anti-GAD Ab Anti-IA-2 Ab Anti-insulin Ab Acetoacetate 3-hydroxybutyrate Acetone Acetone Glucose
Unit
Value
Normal range
% mg/dl mg/dl U/ml U/ml % lmol/l lmol/l lg/ml lg/ml mg/dl
10.8 128.9 3.11 < 0.3 < 0.4 6.7 5 2.0 11844 204.2 201.4 876.7
4.3–5.8 8–22 0.47-0.79 (female) < 1.5 < 0.4 5 7.0 5 55 5 85 0.37–4.69 6.3–33.3 2-20
GAD, glutamic acid decarboxylase; Ab, antibodies; IA, insulinoma associated antigen. Fig. 5. Histopathological examination revealed Periodic acid-Schiff (PAS) stainingpositive nodules in the periphery of the glomerulus of the kidney. Original magnification, 50.
2.3. Physiochemical and toxicological findings The results of the postmortem physiochemical examination are shown in Table 1. The toxicological examination detected no ethanol in the blood or urine. Drug screening of a sample of urine using TriageÒ (Biosite Diagnostics, San Diego, CA, USA) showed no positive findings.
3. Discussion
Fig. 6. Histopathological examination revealed many fat droplets on the basal side of the cytoplasm of proximal tubular epithelium of the kidney (a, HE; b, Oil-Red O). Original magnification, 100.
the periphery of glomerulus, which indicated the finding of nodular glomerulosclerosis (Fig. 5). Oil-Red O staining revealed many fat droplets in the basal side of the cytoplasm of the proximal tubular epithelium of frozen section of the kidney (Fig. 6). In the pancreas, mild fibrosis of islets was found. There were a relatively large number of infiltrating neutrophils in several organs such as the subendocardium of bilateral cardiac ventricles, subcapsule and the portal tract of the liver, spleen, and right kidney. In the thyroid gland, both lobular tumors showed findings of papillary thyroid cancer, which represents well-formed papillary architectures, lined by cells with clear appearing nuclei. No metastatic lesions were observed in the other organs examined. The tumors of the uterus indicated the findings of leiomyoma.
The deceased was found dead in a head-down position. As shown in Fig. 1, the upper parts of the body (head, face, neck, chest and upper extremities) were situated below the rest of the body. Death in a head-down position has been explained by positional (postural) asphyxia and/or by circulatory failure due to marked depletion of venous return [1–10]. Since cases of positional asphyxia usually do not reveal any specific morphological findings at autopsy except for pulmonary edema, visceral congestion, and petechiae of the conjunctivae, viscera, or skin, the following three criteria for diagnosis have been suggested [6–9]: (1) discovery of the decedent in a body position that makes normal breathing impossible and interferes with pulmonary gas change; (2) reasonable explanation that the decedent could not extricate himself/herself from the situation; and (3) other causes of death, both natural and unnatural, must be excluded with a reasonable degree of certainly by autopsy. In this case, the head-down position of the deceased seems to satisfy the criteria (1). The position of the deceased may have compromised respiration because splinting of the chest and diaphragm prevents normal respiratory excursion. In addition, the neck of the deceased was extended. Maximum extension of the neck has been reported to cause airway obstruction [7], although hyperflexed neck is more frequently seen in cases of positional asphyxia [8,9]. As for the criteria (2) and (3) of positional asphyxia, it was rather difficult to determine whether this case met the criteria or not. Positional asphyxia is an exclusion diagnosis that can only be put forward only after the elimination of other possible causes of death [2]. Autopsy revealed papillary thyroid cancers in the thyroid gland. As most papillary cancers are known to be indolent lesions, with 10-year survival rates of up to 95%, especially in patients with no distant metastases [11], we concluded that the cancers did not contribute to her death. Autopsy also revealed extensive hemorrhages of cervical subcutaneous tissues and muscles. These hemorrhages occurred antemortem, since they accompanied relatively marked infiltration of polymorphonuclear leukocytes both within and around the hemorrhages. However, it is probable that the hemorrhages were not
T. Hayashi et al. / Legal Medicine 13 (2011) 196–200
formed by external force against the neck, since autopsy failed to reveal external injuries on the neck or fractures of cervical bone and cartilages. On histopathological examination, Masson–Gomori staining for collagen fibers did not reveal metachromasia of the cutaneous and subcutaneous connective tissue in the skin samples of the neck, which is a marker of compression [12,13]. We concluded that strangulation (hanging or ligature/manual strangulation) was not the cause of death. The postmortem physiochemical examination showed far elevated levels of blood HbA1c (10.8%) and urine glucose (876.7 mg/ dl), which indicates that the deceased suffered from DM with poor control. Blood HbA1c and urine glucose levels are known to retain their stability in postmortem samples [14]. In addition, histopathological examination indicated diabetic glomerulopathy evidenced by glomerulosclerosis in the kidney [11], suggesting a relatively long duration of disease consistent with her past history of illness. Furthermore, most notable findings of physiochemical examinations were highly elevated levels of acetone in both blood (204.2 lg/ml) and urine (201.4 lg/ml), and a high blood concentration of strong acid ketone bodies, in particular 3-hydroxybutyrate increased remarkably (11,844 lmol/l). These findings strongly suggest antemortem DKA. Since anti-glutamic acid decarboxylase (GAD), anti-insulinoma associated antigen-2 (IA-2) and anti-insulin antibodies were not detected, the deceased did not suffer from autoimmune type 1A DM out of type 1 DM (insulin-dependent DM; IDDM). According to her past history of illness and the findings of physiochemical and histopathological examinations [15], it is possible that she suffered from type 2 DM (non-insulin dependent DM; NIDDM). Although DKA occurs classically in young patients with type 1 DM at the time of diagnosis due to absolute insulin insufficiency, it can also occur in older patients with type 2 DM following stress [11]. Stress due to infection, trauma, dehydration, or psychological problems are known to provoke the release of glucose counter regulatory hormones such as catecholamines, glucagon, cortisol, and growth hormone that leads to the development of DKA [14,16,17]. In this case, the histopathological finding of neutrophil infiltration in several organs suggests systemic infectious disease, although the primary focus of the infectious disease could not be found. Moreover, high elevated serum BUN/Cr ratios (41.4; more than 10) suggest antemortem dehydration. Accordingly, systemic infectious disease and/or dehydration was considered to have induced DKA in the deceased. DKA is a severe acute metabolic complication of DM, and the mortality rate in patients with DKA is 5–8% [11,17]. Several cases of sudden unexpected death resulting from DKA have been reported [16–19]. Clinically, the severity of DKA is dependent upon the degree of hyperglycemia and acidosis resulting from the accumulation of acid ketone bodies such as acetoacetate and 3hydroxybutyrate. Iten and Meier [20] reported that postmortem blood levels of b-hydroxybutyrate (3-hydroxybutyrate) are not influenced by postmortem changes within 14 days after death, and that the levels in fatal DKA cases are 2290–37,800 lmol/l (median 22,000; n = 6). Accordingly, blood 3-hydroxybutyrate levels in this case (11,844 lmol/l) were considered to correspond to the values in the case of lethal DKA. In addition, fat droplets in the proximal tubular epithelium, as observed in our case, were observed in subjects who died in a diabetic coma [21,22]. Thus, in this case, the findings suggest that it is possible that the cause of her death was DKA, probably triggered by systemic infectious disease and dehydration. At least, it is certain that DKA is the underlying cause of death. From these findings, a new question arises. Was the direct cause of her death DKA or positional asphyxia? It is possible that she would have died from DKA, even if she was in another position instead of a head-down position. However, the congestion of the head and neck began while she was still alive. The congestion
199
has been described by some authors as ‘hypostasis’, and it may appear as such after death [5]. The polymorphonuclear leukocyte infiltration around the subcutaneous hemorrhages in the neck can develop only when the victim is still alive, and, thus, indicates that the deceased must have survived the formation of the hemorrhages for at least some time [1,3,6]. Numerous petechiae on the palpebral conjunctivae and oral mucosa are formed by an increase of the hydrostatic pressure in the venous system in a head-down position [3,6]. In addition, the hemorrhages in the pectoralis major and minor muscles may occur during the convulsive phase of asphyxia due to effort ventilation [6,10]. These muscles are known to assist respiratory movement. These findings suggest that asphyxia should have arisen while she was alive. Therefore, we conclude that the direct cause of her death was positional asphyxia, and that the deceased satisfied criteria (3). As for criteria (2), reasonable explanation that the decedent could not extricate herself from the situation, there were no findings of either being trapped by extrinsic force or intoxication with alcohol or sedative drugs that are known as the predisposing factors for falling into a confined situation [6–10]. Results of recent studies suggest that underlying organic diseases may also predispose an individual to positional asphyxia [23]. According to the authors, either a loss of consciousness due to cardiovascular disease, cerebrovascular disease, or epilepsy, or a muscle weakness or paralysis due to neurodegenerative diseases such as multiple sclerosis, Parkinson disease, and Lafora disease may generate a susceptibility to positional asphyxia. In the present case, diabetic coma due to severe DKA may explain the inability of self-extrication from the position. We presented a portion of the contents of this article at the 16th Summer Seminar of the Japanese Association of Forensic Pathology, Hakone, August 2009. At the Seminar, we had concluded that the direct cause of death was DKA. Some pathologists’ opinion was that the direct cause of death was positional asphyxia due to DKA, while others suggested that the direct cause was DKA, and positional asphyxia was a contributing factor to her death. According to these opinions, we reanalyzed the skin samples and reconstructed the course of death. As a result, based on the findings described in this article, we reconcluded that the direct cause of her death should be positional asphyxia, which was due to DKA. In conclusion, we present a rare case of death in a head-down position. Based on the findings of histopathological and postmortem physiochemical examinations, as well as autopsy findings, we concluded the direct cause of her death was positional asphyxia resulting from DKA. It is difficult to diagnose a cause of death in unusual posture. The autopsy must be directed towards identifying the precise cause of falling into the posture in order to determine whether or not death was caused by the underling pathological lesions including intoxication. For this purpose, scene photographs are quite useful in confirming a suspicion of positional asphyxia [8,23], in addition to precise autopsy and sufficient examinations, i.e., histopathological, physiochemical, and toxicological examinations.
References [1] Schaefer ATh. Death in a head-down position. In: Tsokos M, editor. Forensic pathology reviews, vol. 3. Totowa: Humana Press; 2005. p. 137–54. [2] Sauvageau A, Desjarlais A, Racette S. Deaths in a head-down position: a case report and review of the literature. Forensic Sci Med Pathol 2008;4:51–4. [3] Madea B. Death in a head-down position. Forensic Sci Int 1993;61:119–32. [4] Purdue B. An unusual accidental death from reverse suspension. Am J Forensic Med Pathol 1992;13:108–11. [5] De Donno A, De Fazio A, Greco MG, Introna F, Maglietta RA. Death in headdown position in a heavily intoxicated obese man. Legal Med 2008;10:204–9. [6] Belviso M, De Donno A, Vitale L, Introna Jr F. Positional asphyxia: reflection on 2 cases. Am J Forensic Med Pathol 2003;24:292–7.
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[7] Padosch SA, Schmidt PH, Kröner LU, Madea B. Death due to positional asphyxia under severe alcoholisation: pathophysiologic and forensic considerations. Forensic Sci Int 2005;149:67–73. [8] Bell MD, Rao VJ, Wetli CV, Rodriguez RN. Positional asphyxiation in adults. A series of 30 cases from the Dade and Broward County Florida Medical Examiner Offices from 1982 to 1990. Am J Forensic Med Pathol 1992;13:101–7. [9] Chan TC, Vilke GM, Neuman T. Reexamination of custody restraint position and positional asphyxia. Am J Forensic Med Pathol 1998;19:201–5. [10] Saukko P, Knight B. Knight’s Forensic Pathology. 3rd ed. London: Arnold; 2004. [11] Maitra A. The endocrine system. In: Kumar V, Abbas AK, Fausto N, Mitchell RN, editors. Robbins basic pathology. Philadelphia: Saunders; 2007. p. 751–800. [12] Janssen W. Forensic histopathology. Berlin: Springer; 1984. [13] Niu WY, Hu JZ, Zhang XM. A new staining method for constriction marks in skin. Forensic Sci Int 1991;50:147–52. [14] Coe JI. Postmortem chemistry update. Emphasis on forensic application. Am J Forensic Med Pathol 1993;14:91–117. [15] Hanafusa T, Imagawa A. Fulminant type 1 diabetes: a novel clinical entity requiring special attention by all medical practitioners. Nat Clin Pract Endocrinol Metab 2007;3:36–45.
[16] Casteels K, Mathieu C. Diabetic ketoacidosis. Rev Endocr Metab Disord 2003;4:159–66. [17] Irwin J, Cohle SD. Sudden death due to diabetic ketoacidosis. Am J Forensic Med Pathol 1988;9:119–21. [18] Yamazaki M, Ogura Y, Wakasugi C, Mitsukuni Y, Yoshimura M. Sudden death due to diabetic coma in insulin-department diabetes mellitus: an autopsy report. Jpn J Leg Med 1997;51:102–10. [19] Yeo KF, Yang YS, Chen KS, Peng CH, Huang CN. Simultaneous presentation of thyrotoxicosis and diabetic ketoacidosis resulted in sudden cardiac arrest. Endocr J 2007;54:991–3. [20] Iten PX, Meier M. Beta-hydroxybutyric acid – an indicator for an alcoholic ketoacidosis as cause of death in deceased alcohol abusers. J Forensic Sci 1999;45:624–32. [21] Thomsen JL, Hansen TP. Lipids in the proximal tubules of the kidney in diabetic coma. Am J Forensic Med Pathol 2000;21:416–8. [22] Nielsen H, Thomsen JL, Kristensen IB, Ottosen PD. Accumulation of triglycerides in the proximal tubule of the kidney in diabetic coma. Pathology 2003;35:305–10. [23] Byard RW, Wick R, Gilbert JD. Conditions and circumstances predisposing to death from positional asphyxia in adults. J Forensic Leg Med 2008;15:415–9.
Contents lists available at ScienceDirect
Legal Medicine journal homepage: www.elsevier.com/locate/legalmed
Case Report
Positional asphyxia or diabetic ketoacidosis? A case report Takahito Hayashi ⇑, Kazutoshi Ago, Mihoko Ago, Mamoru Ogata Department of Legal Medicine, Graduate School of Medical and Dental Sciences, Kagoshima University, 8-35-1 Sakuragaoka, Kagoshima 890-8544, Japan
a r t i c l e
i n f o
Article history: Received 25 December 2010 Received in revised form 27 January 2011 Accepted 31 January 2011 Available online 4 March 2011 Keywords: Diabetic ketoacidosis (DKA) Head-down position Positional asphyxia Diabetes mellitus Forensic pathology Cause of death
a b s t r a c t We describe an autopsy case in which a patient with diabetic ketoacidosis (DKA) was found in a headdown position. A female in her late 70s was found dead in her home in a supine position on the kitchen floor. The upper part of her body was hanging down over the edge of the kitchen floor to the backyard through the open window. External examination revealed congestion of the head and upper region of the face and neck. There were numerous petechiae on the superior palpebral conjunctivae and upper part of the oral mucosa. On internal examination, extensive hemorrhages in the subcutaneous fat tissues and muscles were observed at the upper part of the neck, although there were no external injuries on the neck. Histopathological examination revealed that hemorrhages were accompanied with infiltration of polymorphonuclear leukocytes both within and around the hemorrhages on the neck skin. Nodular glomerulosclerosis and many fat droplets in the cytoplasm of proximal tubule cells were found in the kidney. Postmortem blood analysis showed acetone (204.2 lg/ml), HbA1c (10.8%), acetoacetate (<2.0 lmol/ l), 3-hydroxybutyrate (11,844 lmol/l), blood urea nitrogen (128.9 mg/dl), and creatinine (3.11 mg/dl). The glucose and acetone levels in the urine were 876.7 mg/dl and 201.4 lg/ml, respectively, suggesting that she suffered severe DKA. However, since hemorrhage of the neck could have developed only when she was still alive, asphyxia should have arisen antemortem. Based on these findings, we concluded that the direct cause of her death is positional asphyxia, which was resulted from DKA. It is difficult to diagnose the cause of death when the victim is in an unusual posture. To confirm a suspicion of positional asphyxia, photographs of the undisturbed scene are useful in addition to a precise autopsy and accurate examinations. Ó 2011 Elsevier Ireland Ltd. All rights reserved.
1. Introduction An increased incidence of death in a head-down position has been reported [1–5]. Common features in these cases include (a) the body in an inverted or head-down tilted position, (b) marked congestion of the face, scalp, neck, and other dependent parts of the body (hands and shoulders), (c) accompanying effects of the internal congestion with swelling of and petechial bleedings at the affected parts, as well as edema of the brain and lungs, and (d) lack of a definite pathoanatomical cause of death [1]. Although the pathophysiology of death in a head-down position is not fully understood, several previous reports suggest that death results from asphyxia due to fixation of the chest with hindering of thoracic movements and ventilation, and/or by circulatory failure due to marked depletion of the venous return to the heart [2–4]. Asphyxia caused by the adoption of particular positions in relation to unusual body posture that mechanically interferes with pulmonary ventilation is called ‘‘positional (postural) asphyxia’’ [6– 10]. However, it is often difficult to diagnose the cause of death ⇑ Corresponding author. Tel.: +81 99 275 5313; fax: +81 99 275 5315. E-mail address: [email protected] (T. Hayashi). 1344-6223/$ - see front matter Ó 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.legalmed.2011.01.006
in such cases because they generally present with an aspecific pathoanatomical picture [5,6]. In this report, we describe a case of death in a head-down position in a patient with diabetic ketoacidosis (DKA), and discuss the cause of death and the relationship of the position of the body to the death. 2. Case report A female in her late 70s was found dead in her home, lying naked except for a shirtwaist in a supine position on the kitchen floor with the upper part of her body hanging out of the open window to the backyard (Fig. 1). She bent her back and the upper part of her body including the head, face, neck, chest and upper extremities was situated below the kitchen floor. The left and right hands reached to the ground which was approximately 70 cm lower than the kitchen floor, whereas the head was hanging down loosely. Although the right upper extremity was found in a garbage box on the backyard, she was not wedged in a confined space. The lumber region was just situated on the windowsill (the edge of kitchen floor), and the gluteal region and both lower extremities spread apart were positioned on the kitchen floor. Although some
T. Hayashi et al. / Legal Medicine 13 (2011) 196–200
Fig. 1. Deceased at the scene.
underclothes, toilet papers and vomitus lay scattered on the floor around her, there were no objects that fixed the lower part of her body on the floor. Her position was not fixed by any forces. However, it was supposed that the position was stable, since the sacral region that corresponded to center of gravity of her body was left being on the kitchen floor. She was seen alive 2 days before. Police investigations revealed that she was diagnosed with type 2 diabetes mellitus (DM) approximately 10 years prior to death, but that she did not follow the medical service. An autopsy was carried out at approximately 2.5 days after death. 2.1. Autopsy findings The deceased was 145.0 cm tall and weighed 40.0 kg. External examination revealed dark purple-red discoloration of the head, upper region of the face and neck (Fig. 2). Numerous petechiae were found particularly on the superior palpebral conjunctivae and upper part of the oral mucosa. There were small abrasions and bruises on the back, and the upper and lower extremities. Internal examination revealed extensive hemorrhage of subcutaneous tissues of the neck (Fig. 3), although no external injuries were found on the neck. Hemorrhages were also noted in the cervical muscles such as platysma, left digastric muscle, bilateral mylohyoid muscles, and bilateral cricothyroid muscles. Those
Fig. 2. Congestion of the upper region of the face.
197
Fig. 3. Internal examinations of the neck. Hemorrhages of subcutaneous tissues were observed.
hemorrhages in soft tissues were localized predominantly to the upper part of the neck. No fractures of the hyoid bone, thyroid or cricoid cartilage were observed. Spotty subfascial hemorrhages in the left and right pectoralis major and minor muscles were observed. The brain weighed 1,220 g, and moderate edema was noted. Neither cerebral contusion nor hemorrhage was observed. The heart weighed 340 g, and many subepicardial petechiae were seen. A large amount of dark-red fluid blood mixed with fat-like and soft coagulated blood, was retained in the heart. Slight atherosclerosis was found on the coronary arteries. The left and right lungs weighed 310 g and 390 g, respectively, and both showed congestion. In the left and right lobe of the thyroid gland, solid tumors (3.0 1.4 1.5 cm, 2.5 2.0 1.5 cm in size, respectively) were found. There was a sharply circumscribed solid tumor (3.5 2.8 2.8 cm in size) in the left wall of the uterus. There were no remarkable findings in other organs except for congestion.
2.2. Histopathological findings Extensive hemorrhages accompanied with relatively marked infiltration of polymorphonuclear leukocytes both within and around the hemorrhages were found in the subcutaneous tissue of the neck skin (Fig. 4). Masson–Gomori staining for collagen fibers did not detect metachromasia of the cutaneous and subcutaneous connective tissue of the neck. There was small patchy loss of cardiac muscle cells in the left and right ventricles. In the kidney, PAS (Periodic acid-Schiff) staining-positive nodules were found in
Fig. 4. Histopathological examination revealed subcutaneous hemorrhages accompanied with relatively marked infiltration of polymorphonuclear leukocytes both within and around the hemorrhages of left lateral cervical region (HE). Original magnification, 50.
198
T. Hayashi et al. / Legal Medicine 13 (2011) 196–200 Table 1 Data obtained from the postmortem physiochemical examination. Material Blood Serum Serum Serum Serum Serum Serum Serum Blood Urine Urine
Hemoglobin A1c Blood urea nitrogen Creatinine Anti-GAD Ab Anti-IA-2 Ab Anti-insulin Ab Acetoacetate 3-hydroxybutyrate Acetone Acetone Glucose
Unit
Value
Normal range
% mg/dl mg/dl U/ml U/ml % lmol/l lmol/l lg/ml lg/ml mg/dl
10.8 128.9 3.11 < 0.3 < 0.4 6.7 5 2.0 11844 204.2 201.4 876.7
4.3–5.8 8–22 0.47-0.79 (female) < 1.5 < 0.4 5 7.0 5 55 5 85 0.37–4.69 6.3–33.3 2-20
GAD, glutamic acid decarboxylase; Ab, antibodies; IA, insulinoma associated antigen. Fig. 5. Histopathological examination revealed Periodic acid-Schiff (PAS) stainingpositive nodules in the periphery of the glomerulus of the kidney. Original magnification, 50.
2.3. Physiochemical and toxicological findings The results of the postmortem physiochemical examination are shown in Table 1. The toxicological examination detected no ethanol in the blood or urine. Drug screening of a sample of urine using TriageÒ (Biosite Diagnostics, San Diego, CA, USA) showed no positive findings.
3. Discussion
Fig. 6. Histopathological examination revealed many fat droplets on the basal side of the cytoplasm of proximal tubular epithelium of the kidney (a, HE; b, Oil-Red O). Original magnification, 100.
the periphery of glomerulus, which indicated the finding of nodular glomerulosclerosis (Fig. 5). Oil-Red O staining revealed many fat droplets in the basal side of the cytoplasm of the proximal tubular epithelium of frozen section of the kidney (Fig. 6). In the pancreas, mild fibrosis of islets was found. There were a relatively large number of infiltrating neutrophils in several organs such as the subendocardium of bilateral cardiac ventricles, subcapsule and the portal tract of the liver, spleen, and right kidney. In the thyroid gland, both lobular tumors showed findings of papillary thyroid cancer, which represents well-formed papillary architectures, lined by cells with clear appearing nuclei. No metastatic lesions were observed in the other organs examined. The tumors of the uterus indicated the findings of leiomyoma.
The deceased was found dead in a head-down position. As shown in Fig. 1, the upper parts of the body (head, face, neck, chest and upper extremities) were situated below the rest of the body. Death in a head-down position has been explained by positional (postural) asphyxia and/or by circulatory failure due to marked depletion of venous return [1–10]. Since cases of positional asphyxia usually do not reveal any specific morphological findings at autopsy except for pulmonary edema, visceral congestion, and petechiae of the conjunctivae, viscera, or skin, the following three criteria for diagnosis have been suggested [6–9]: (1) discovery of the decedent in a body position that makes normal breathing impossible and interferes with pulmonary gas change; (2) reasonable explanation that the decedent could not extricate himself/herself from the situation; and (3) other causes of death, both natural and unnatural, must be excluded with a reasonable degree of certainly by autopsy. In this case, the head-down position of the deceased seems to satisfy the criteria (1). The position of the deceased may have compromised respiration because splinting of the chest and diaphragm prevents normal respiratory excursion. In addition, the neck of the deceased was extended. Maximum extension of the neck has been reported to cause airway obstruction [7], although hyperflexed neck is more frequently seen in cases of positional asphyxia [8,9]. As for the criteria (2) and (3) of positional asphyxia, it was rather difficult to determine whether this case met the criteria or not. Positional asphyxia is an exclusion diagnosis that can only be put forward only after the elimination of other possible causes of death [2]. Autopsy revealed papillary thyroid cancers in the thyroid gland. As most papillary cancers are known to be indolent lesions, with 10-year survival rates of up to 95%, especially in patients with no distant metastases [11], we concluded that the cancers did not contribute to her death. Autopsy also revealed extensive hemorrhages of cervical subcutaneous tissues and muscles. These hemorrhages occurred antemortem, since they accompanied relatively marked infiltration of polymorphonuclear leukocytes both within and around the hemorrhages. However, it is probable that the hemorrhages were not
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formed by external force against the neck, since autopsy failed to reveal external injuries on the neck or fractures of cervical bone and cartilages. On histopathological examination, Masson–Gomori staining for collagen fibers did not reveal metachromasia of the cutaneous and subcutaneous connective tissue in the skin samples of the neck, which is a marker of compression [12,13]. We concluded that strangulation (hanging or ligature/manual strangulation) was not the cause of death. The postmortem physiochemical examination showed far elevated levels of blood HbA1c (10.8%) and urine glucose (876.7 mg/ dl), which indicates that the deceased suffered from DM with poor control. Blood HbA1c and urine glucose levels are known to retain their stability in postmortem samples [14]. In addition, histopathological examination indicated diabetic glomerulopathy evidenced by glomerulosclerosis in the kidney [11], suggesting a relatively long duration of disease consistent with her past history of illness. Furthermore, most notable findings of physiochemical examinations were highly elevated levels of acetone in both blood (204.2 lg/ml) and urine (201.4 lg/ml), and a high blood concentration of strong acid ketone bodies, in particular 3-hydroxybutyrate increased remarkably (11,844 lmol/l). These findings strongly suggest antemortem DKA. Since anti-glutamic acid decarboxylase (GAD), anti-insulinoma associated antigen-2 (IA-2) and anti-insulin antibodies were not detected, the deceased did not suffer from autoimmune type 1A DM out of type 1 DM (insulin-dependent DM; IDDM). According to her past history of illness and the findings of physiochemical and histopathological examinations [15], it is possible that she suffered from type 2 DM (non-insulin dependent DM; NIDDM). Although DKA occurs classically in young patients with type 1 DM at the time of diagnosis due to absolute insulin insufficiency, it can also occur in older patients with type 2 DM following stress [11]. Stress due to infection, trauma, dehydration, or psychological problems are known to provoke the release of glucose counter regulatory hormones such as catecholamines, glucagon, cortisol, and growth hormone that leads to the development of DKA [14,16,17]. In this case, the histopathological finding of neutrophil infiltration in several organs suggests systemic infectious disease, although the primary focus of the infectious disease could not be found. Moreover, high elevated serum BUN/Cr ratios (41.4; more than 10) suggest antemortem dehydration. Accordingly, systemic infectious disease and/or dehydration was considered to have induced DKA in the deceased. DKA is a severe acute metabolic complication of DM, and the mortality rate in patients with DKA is 5–8% [11,17]. Several cases of sudden unexpected death resulting from DKA have been reported [16–19]. Clinically, the severity of DKA is dependent upon the degree of hyperglycemia and acidosis resulting from the accumulation of acid ketone bodies such as acetoacetate and 3hydroxybutyrate. Iten and Meier [20] reported that postmortem blood levels of b-hydroxybutyrate (3-hydroxybutyrate) are not influenced by postmortem changes within 14 days after death, and that the levels in fatal DKA cases are 2290–37,800 lmol/l (median 22,000; n = 6). Accordingly, blood 3-hydroxybutyrate levels in this case (11,844 lmol/l) were considered to correspond to the values in the case of lethal DKA. In addition, fat droplets in the proximal tubular epithelium, as observed in our case, were observed in subjects who died in a diabetic coma [21,22]. Thus, in this case, the findings suggest that it is possible that the cause of her death was DKA, probably triggered by systemic infectious disease and dehydration. At least, it is certain that DKA is the underlying cause of death. From these findings, a new question arises. Was the direct cause of her death DKA or positional asphyxia? It is possible that she would have died from DKA, even if she was in another position instead of a head-down position. However, the congestion of the head and neck began while she was still alive. The congestion
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has been described by some authors as ‘hypostasis’, and it may appear as such after death [5]. The polymorphonuclear leukocyte infiltration around the subcutaneous hemorrhages in the neck can develop only when the victim is still alive, and, thus, indicates that the deceased must have survived the formation of the hemorrhages for at least some time [1,3,6]. Numerous petechiae on the palpebral conjunctivae and oral mucosa are formed by an increase of the hydrostatic pressure in the venous system in a head-down position [3,6]. In addition, the hemorrhages in the pectoralis major and minor muscles may occur during the convulsive phase of asphyxia due to effort ventilation [6,10]. These muscles are known to assist respiratory movement. These findings suggest that asphyxia should have arisen while she was alive. Therefore, we conclude that the direct cause of her death was positional asphyxia, and that the deceased satisfied criteria (3). As for criteria (2), reasonable explanation that the decedent could not extricate herself from the situation, there were no findings of either being trapped by extrinsic force or intoxication with alcohol or sedative drugs that are known as the predisposing factors for falling into a confined situation [6–10]. Results of recent studies suggest that underlying organic diseases may also predispose an individual to positional asphyxia [23]. According to the authors, either a loss of consciousness due to cardiovascular disease, cerebrovascular disease, or epilepsy, or a muscle weakness or paralysis due to neurodegenerative diseases such as multiple sclerosis, Parkinson disease, and Lafora disease may generate a susceptibility to positional asphyxia. In the present case, diabetic coma due to severe DKA may explain the inability of self-extrication from the position. We presented a portion of the contents of this article at the 16th Summer Seminar of the Japanese Association of Forensic Pathology, Hakone, August 2009. At the Seminar, we had concluded that the direct cause of death was DKA. Some pathologists’ opinion was that the direct cause of death was positional asphyxia due to DKA, while others suggested that the direct cause was DKA, and positional asphyxia was a contributing factor to her death. According to these opinions, we reanalyzed the skin samples and reconstructed the course of death. As a result, based on the findings described in this article, we reconcluded that the direct cause of her death should be positional asphyxia, which was due to DKA. In conclusion, we present a rare case of death in a head-down position. Based on the findings of histopathological and postmortem physiochemical examinations, as well as autopsy findings, we concluded the direct cause of her death was positional asphyxia resulting from DKA. It is difficult to diagnose a cause of death in unusual posture. The autopsy must be directed towards identifying the precise cause of falling into the posture in order to determine whether or not death was caused by the underling pathological lesions including intoxication. For this purpose, scene photographs are quite useful in confirming a suspicion of positional asphyxia [8,23], in addition to precise autopsy and sufficient examinations, i.e., histopathological, physiochemical, and toxicological examinations.
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