Death Caused by Cardioinhibitory Reflex

ORIGINAL ARTICLE

Death Caused by Cardioinhibitory Reflex What Experts Believe Bettina Schrag, MD, Patrice Mangin, MD, PhD, Paul Vaucher, MSc, and Marc D. Bollmann, MD Abstract: The danger of neck compression without restriction of the arterial flow remains unresolved in forensic medicine. There is an ongoing debate concerning life endangerment due to the cardioinhibitory reflex. The aim of this study was to determine what forensic medical experts believe and how they deal with this reflex. An anonymous electronic questionnaire was sent to 1429 forensic medical experts all over the world. We asked them about their opinion on the cardioinhibitory reflex, its role in causing death, and what their diagnostic criteria were. A total of 182 questionnaires were returned. The experts who answered were from 32 different countries. Our survey showed that 80.2% of experts believe that the cardioinhibitory reflex can theoretically cause death. In the practical application opinions diverge though. Apparently, the practical application mainly depends on the habit of the individual expert. We observed no consensus on the diagnostic criteria to be used. Given the potentially frequent use of the concept of the cardioinhibitory reflex in forensic practice and its judicial impact it would be important to reach a consensus.

an arterial baroreflex controlling the heart rate (baroreflex syncope). There is however an ongoing debate concerning life endangerment in clinical forensic medicine due to this mechanism. We have therefore conducted an international survey among forensic physicians and pathologists to study, if and how the cardioinhibitory reflex is routinely used in their expert opinions.

MATERIALS AND METHODS

Manuscript received September 11, 2009; accepted September 27, 2009. From the University Centre of Legal Medicine, Western Switzerland, GenevaLausanne, Lausanne, Switzerland. Supported by the University Centre of Legal Medicine, Western Switzerland, Lausanne. The authors report no conflicts of interest. Reprints: Bettina Schrag, MD, Rue Michel-Servet 1, 1211 Geneva 4, Switzerland. E-mail: [email protected]. Copyright * 2012 by Lippincott Williams & Wilkins ISSN: 0195-7910/12/3301Y0008 DOI: 10.1097/PAF.0b013e3181db7efd

We set up a web-based anonymous survey addressed to worldwide forensic experts. The primary objectives of this study were to assess the prevalence of forensic experts who believe that the cardioinhibitory reflex can cause death, and the prevalence of those who have practically attributed death or life endangerment to this reflex. Secondary objectives were to compare the characteristics (age, gender, origin, training, experience) of the experts with their stated opinions, to describe the different diagnostic criteria that are used, and finally to test the internal consistency of reported opinions. An anonymous electronic questionnaire was sent to 1429 forensic experts all over the world in May and June 2007. The solicited experts were found through the member listings of the International Academy of Legal Medicine (n = 319), the National Association of Medical Examiners (NAME; n = 781), the American Association of Forensic Sciences (n = 94; only non-American members, since they have been contacted through the NAME) and the French (n = 250), Swiss (n = 48), and German (n = 31) associations of legal medicine. Some scientific societies had e-mail distribution lists, whereas other e-mail addresses had to be manually searched for. An additional 14 questionnaires were collected from experts during the AAFS International Congress in 2008. All the other answers were anonymously returned over the Internet and were collected on a protected server of the University of Lausanne, Switzerland. In the survey, we asked the experts_ personal opinions on the lethality of the cardioinhibitory reflex, and how they dealt with the cardioinhibitory reflex practically in forensic pathology and in clinical forensic medicine. Five possible diagnostic criteria were proposed. Data collected in the survey included the demographics and professional background of the participants and the annual number of cases of cardioinhibitory reflex that they encountered. Names and mail addresses of the forensic experts were obtained from the distribution lists of the French and Swiss societies of legal medicine and the international academy of Legal Medicine. The members of the NAME were contacted through their secretary. E-mail addresses of the experts on the international listings of the American Association of Forensic Sciences and of the German Association of Legal Medicine were found on the Internet. Prevalence of experts believing cardioinhibitory reflex can cause death or be life threatening, and the prevalence of those having practically attributed such a diagnosis were reported with a 95% confidence interval (95% CI). The significance level was set at 0.05 to detect characteristic differences between those who believe cardioinhibitory reflex can cause death and

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Key Words: neck trauma, death, sudden, baroreflex, carotid, cardioinhibitory (Am J Forensic Med Pathol 2012;33: 8Y12)

T

he cardioinhibitory reflex, an arterial baroreflex controlling the heart rate, is well described in the literature and its existence is uncontested. It is also the basis of therapeutic and diagnostic techniques that are often used in cardiology. The arterial baroreflex represents a fundamental physiologic mechanism of cardiovascular homeostasis.1Y11 Among the first authors who reported that a compression of the side of the neck can lead to a circulatory collapse were Parry, Waller, and Landois in the 18th and 19th century.5 However, they gave no pathophysiological explanation for the phenomenon. Czermak12 in 1866 thought that it was due to a direct excitation of the vagal nerve. Hering13 in 1924 observed, on animal experiments, that the compression of the neck slowed the heart rate, and he explained this observation by a mechanical excitation of the carotid sinus, so describing the arterial baroreflex. Franke delineated in his papers the 3 different response-types of the stimulation of the carotid sinus with huge interindividual variations.12,14 The actual danger of neck compression due to the baroreceptor reflex alone (without obstruction of the arteries) remains unresolved in the forensic medical practice. It is generally accepted that a blow or a short compression of the side of the neck can lead to a circulatory collapse due to the activation of

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Volume 33, Number 1, March 2012

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Reported Death by Cardioinhibitory Reflex

those who do not. Exact Fisher exact test was used for binomial variables and W2 test for variable with more than 2 issues. Consistency between opinions regarding death or life endangerment was tested using kappa statistic with 95% CI.

14 additional questionnaires were collected during an international meeting. One questionnaire was submitted empty; 182 were included in the analysis. Responses came from experts from 32 countries throughout the world (Table 1). The prevalence of forensic experts who believe that death can be caused by a cardioinhibitory reflex was of 80.2% (95% CI: 73.7, 85.7). The others (n = 32) either had no opinion (n = 18, 9.9%) or rejected this possibility (n = 18, 9.9%). We did not observe any significant differences in the physicians_

RESULTS From the initial 1429 e-mail addresses, 49 e-mail addresses were invalid. Hence 1380 forensic specialists were invited to participate and 169 accessed the web-based questionnaire and

TABLE 1. Physicians’ Characteristics Between Those Who Believe Cardioinhibitory Reflex Can Cause Death and Those That Do Not Characteristics

Total n = 182

Age G35 yr 35Y49 yr 50Y64 yr Q65 yr Sex Male Female Country† USA Other America Germany France Switzerland Italy/Spain/Portugal Other Europe Asia/Oceania/Africa Degree MD or DO PhD or MSc Professor or associate professor Years of experience e10 11Y20 21Y30 930 Autopsies per year None G50 50Y99 100Y199 200Y499 Q500 Clinical investigations per year None G50 50Y99 100Y199 200Y499 Q500

Believing n = 146

Unbelieving n = 36

P* P = 0.387

17 (9.3%) 82 (45.0%) 60 (33.0%) 23 (12.7%)

11 (7.5%) 66 (45.2%) 50 (34.3%) 19 (13.0%)

6 (16.7%) 16 (44.4%) 10 (27.8%) 4 (11.1%)

143 (78.6%) 39 (21.4%)

114 (78.1%) 32 (21.9%)

29 (80.6%) 7 (19.4%)

P = 0.824

P = 0.323† 55 (30.2%) 8 (4.4%) 17 (9.3%) 8 (4.4%) 32 (17.6%) 24 (13.2%) 27 (14.8%) 11 (6.0%)

42 (28.7%) 8 (8.9%) 13 (8.9%) 5 (3.4%) 28 (19.2%) 22 (15.1%) 21 (14.4%) 7 (4.8%)

13 (36.1%) 0 (0.0%) 4 (11.1%) 3 (8.3%) 4 (11.1%) 2 (5.6%) 6 (16.7%) 4 (11.1%)

102 (56.0%) 28 (15.4%) 52 (28.6%)

81 (55.5%) 20 (13.7%) 45 (30.8%)

21 (58.3%) 8 (22.2%) 7 (19.4%)

53 (29.3%) 62 (34.2%) 40 (22.1%) 26 (14.4%)

40 (27.6%) 49 (33.8%) 35 (24.1%) 21 (14.5%)

13 (36.1%) 13 (36.1%) 5 (13.9%) 5 (13.9%)

62 (34.1%) 8 (4.4%) 19 (10.4%) 38 (20.9%) 48 (26.4%) 7 (3.8%)

48 (32.9%) 6 (4.1%) 14 (9.6%) 32 (21.9%) 40 (27.4%) 6 (4.1%)

14 (38.9%) 2 (5.5%) 5 (13.9%) 6 (16.7%) 8 (22.2%) 1 (2.8%)

P = 0.257

P = 0.544

P = 0.881

P = 0.481 124 (68.1%) 25 (13.7%) 9 (5.0%) 7 (3.9%) 12 (6.6%) 5 (2.7%)

102 (69.9%) 20 (13.7%) 8 (5.5%) 4 (2.7%) 8 (5.5%) 4 (2.7%)

22 (61.1%) 5 (13.9%) 1 (2.8%) 3 (8.3%) 4 (11.1%) 1 (2.8%)

*P values are calculated using Fisher exact test for binomial variables and W2 test for nonbinomial variables. † 2 W was computed regrouping countries through continents. Asia, Africa, and Oceania were grouped.

* 2012 Lippincott Williams & Wilkins



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TABLE 2. Basis for Attributing Death to Cardioinhibitory Reflex Cardiac Arrest According to Experts Who Have at Least Once Reported Such a Case (n = 81) Sequence of Events

By Exclusion X X X X

X X X X X X

X

X X

Macroscopic Examination

Microscopic Examination

X X

X X

X X X X

X X X

X

X

X

X X

Complementary Investigations

X

X X X

X X

X X 57 (70.4%)

56 (69.1%)

X 44 (54.3%)

characteristics between those who believe cardioinhibitory reflex can cause death and those who do not (Table 1). Concerning the practical application of the cardioinhibitory reflex in their postmortem casework, 81 of 174 forensic

X X X X 38 (46.9%)

X X X X 20 (24.7%)

N (%) 13 (16.0%) 12 (14.8%) 12 (14.8%) 9 (11.1%) 6 (7.4%) 6 (7.4%) 5 (6.2%) 4 (4.9%) 3 (3.7%) 2 (2.5%) 2 (2.5%) 1 (1.2%) 1 (1.2%) 1 (1.2%) 1 (1.2%) 1 (1.2%) 1 (1.2%) 1 (1.2%) 81 (100%)

experts (46.6%; 95% CI: 39.0, 54.3) had attributed at least one death to a cardioinhibitory reflex triggered by a neck injury or compression. Concerning the clinical casework, 71 of 168 experts (42.3%; 95% CI: 34.7, 50.1) had ascribed life

TABLE 3. Basis for Attributing Life Endangerment Due to Cardioinhibitory Reflex Cardiac Following Neck Trauma According to Experts Who Have at Least Once Reported Such a Case (n = 71) Sequence of Events X X X

By Exclusion

Subjective Findings

Objective Findings

Complementary Investigations

X X X

X

X

X

X X X

X X X

X

X

X

X X

X X

X

X

X

X

X X

X X

X X X X

X

54 (76.1%)

10

X

X X X X X

X

X

X X

37 (52.1%)

31 (43.7%)

36 (50.7%)


X X

24 (33.8%)

N (%) 9 (12.7%) 8 (11.3%) 8 (11.3%) 7 (9.9%) 7 (9.9%) 5 (7.0%) 5 (7.0%) 3 (4.2%) 3 (4.2%) 3 (4.2%) 2 (2.8%) 2 (2.8%) 2 (2.8%) 1 (1.4%) 1 (1.4%) 1 (1.4%) 1 (1.4%) 1 (1.4%) 1 (1.4%) 1 (1.4%) 71 (100%)




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endangerment to the cardioinhibitory reflex in an expert opinion. Nineteen experts (10.4%) contemplated the possibility of death or life endangerment at least once in a year. We did not observe any consensus about the diagnostic criteria that were used by the different experts. Tables 2 and 3 illustrate the diagnostic criteria the experts used to attribute death or life endangerment to this reflex. Experts_ working in clinical forensic medicine based their diagnosis on 20 different combinations of the 5 proposed diagnostic criteria. Accordingly the experts performing autopsies used 18 different combinations of diagnosing death due to the cardioinhibitory reflex. Finally, the physicians_ opinions about cardioinhibitory reflex being able to cause death were compared with their belief about the cardioinhibitory reflex following neck compression endangering life. Most physicians (88.5%) gave a consistent answer to both questions (kappa = 0.65; 95% CI: 0.51, 0.79). However, 12 physicians (6.6%) considered cardioinhibitory reflex to be able to cause death without considering it as a cause of life endangerment, and 9 (4.9%) believed it to endanger life rejected it as a cause death.

The main limitation of this study is the low response rate which was of only 13.2%. We have no way of testing whether nonresponders would show similar characteristics to those who answered our survey. Another limitation is the inconsistency of responses with the experts_ opinion. This has been discussed during scientific meetings, where experts who were surprised by the results have explained their inconsistent opinions: they mainly took into account their past expert opinions without questioning the content in the light of their actual views. Our survey results show that the significance of the cardioinhibitory reflex is theoretically widely accepted. However, in practice, we did not find a uniform application. Given the frequent use of the concept of the cardioinhibitory reflex in forensic practice and the variability of diagnostic criteria and interpretation, finding a consensus is important. The cardioinhibitory reflex as a cause of death or as a life-endangering factor should nevertheless be used with caution, also considering the scarceness of well-documented cases. In practice, the association between cardioinhibitory reflex and death remains difficult or even impossible to prove.

DISCUSSION A large majority of forensic physicians believe that the cardioinhibitory reflex can cause death (80.2%). Believers and unbelievers are found in all countries, among experts of all academic degrees. Our results therefore suggest that the experts_ beliefs are not based on common guidelines and do not depend on the judicial systems. Even though the cardioinhibitory reflex is theoretically believed to be potentially deadly its application in practice is controversial. Contrary to their theoretical opinion, only 42.3% of the forensic pathologists use it as a cause of death and 42.3% ascribe life endangerment to it in their clinical forensic practice. The diagnostic criteria however vary considerably and no consensus could be observed. The 81 pathologists who use cardioinhibitory reflex as a cause of death reported 18 different combinations of the suggested diagnostic criteria to attribute death and forensic physicians reported 20 combinations to attribute life endangerment. A number of physicians (30.8%) make the diagnosis by exclusion of other causes of death. Given the potential judicial consequences of such a decision one would rather expect that the diagnosis should be based on objective findings.15 Even though most experts did not challenge the significance of the cardioinhibitory reflex in forensic pathology and in clinical forensic medicine, only about half of the responders use it in practice. Taken together with the discrepancies in the diagnostic criteria, our survey cannot detect a usable mainstream opinion. Looking more closely at the scientific evidence, only few authors mention that a short compression of the side of the neck causes death, probably due to a baroreflex. Well-known and often cited case reports of death following neck compression include those by Lochte and Dyrenfurth, Giese, Esser and Simpson.16Y20 These case reports are not very detailed. In 1989, Sigrist published a series of 7 cases of short-termed neck trauma each one with a short interval between trauma and death. In each case, he observed injuries of the carotid bifurcation. Based on his observations, he postulated a persistence of the baroreflex-like stimulation even after the initial trauma as the cause of death.21 According to that, Bolliger has recently reported a case of a deadly broomstick trauma.15 However, in our survey, 40.7% of experts who have attributed death to cardioinhibitory reflex do not consider local findings for their diagnosis. A consensus on the diagnostic criteria to be used based on the existing literature could be very helpful for forensic experts. * 2012 Lippincott Williams & Wilkins

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15. Bolliger S, Plattner T, Zollinger U. The deadly broomstick: an unusual missile injury to the neck. Am J Forensic Med Pathol. 2006;27:304Y306.

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20. Simpson K. Deaths from vagal inhibition. Lancet. 1949;1:558Y560. 21. Sigrist T, Meier K, Zollinger U. Traumatic carotid sinus reflex death. Beitr Gerichtl Med. 1989;47:257Y266.

