Author + information
- Received May 4, 2016
- Revision received June 14, 2016
- Accepted June 14, 2016
- Published online September 20, 2016.
- Sunil K. Sinha, MDa,∗ (, )
- Barbara Crain, MD, PhDb,
- Katie Flickinger, MSb,
- Hugh Calkins, MDa,
- John Rickard, MDc,
- Alan Cheng, MDa,
- Ronald Berger, MD, PhDa,
- Gordon Tomaselli, MDa and
- Joseph E. Marine, MDa
- aDivision of Cardiology, Johns Hopkins University School of Medicine, Baltimore, Maryland
- bDepartment of Pathology, Johns Hopkins University School of Medicine, Baltimore, Maryland
- cDepartment of Cardiovascular Medicine, Cleveland Clinic, Cleveland, Ohio
- ↵∗Reprint requests and correspondence:
Dr. Sunil K. Sinha, Division of Cardiology, The Johns Hopkins Hospital, 600 North Wolfe Street, Halsted 502, Baltimore, Maryland 21287-0409.
Background Cardiovascular implantable electronic device (CIED) removal and interrogation are recommended at autopsy in suspected cases of sudden cardiac death, but data on the role of nonselective post-mortem CIED (pacemaker or defibrillator) analysis in this setting are lacking.
Objectives This study undertook an institutional registry analysis to determine the utility of systematic routine CIED removal, interrogation, and analysis at autopsy.
Methods From May 19, 2009, to May 18, 2015, autopsy subjects with a CIED at a Johns Hopkins University medical institution (Baltimore, Maryland) underwent CIED removal and interrogation by an electrophysiologist for clinical alerts. The CIED was then submitted for technical analysis by the manufacturer. The CIED interrogation, the manufacturer’s technical analysis, and the final autopsy report were all cataloged in the Johns Hopkins Post-mortem CIED Registry.
Results A total of 2,025 autopsies were performed; 84 subjects had CIEDs removed and analyzed. These devices included 37 pacemakers and 47 defibrillators. Overall, 43 subjects had died suddenly, and 41 had not died suddenly. Significant clinical alerts (sustained tachyarrhythmias or an elevated fluid index value) were seen in 62.8% cases of sudden deaths. In the nonsudden death cohort, 19.5% displayed a significant clinical alert. Significant association of CIED alerts were noted when comparing sudden deaths versus nonsudden deaths (p < 0.001), defibrillators versus pacemakers (p < 0.005), and cardiac versus noncardiac causes of death (p < 0.001). Manufacturer analyses revealed a case of premature pacemaker battery depletion, as well as a hard reset in a defibrillator as a result of cold exposure.
Conclusions Post-mortem CIED analysis was clinically useful in assisting with determination of the timing, mechanism, and cause of death in the majority of sudden deaths and in almost 20% of nonsudden deaths. The authors advocate CIED removal with analysis as an important diagnostic tool in all autopsies and to assist manufacturers in identifying potentially fatal device failures.
Cardiovascular implantable electronic devices (CIEDs) encompass permanent pacemakers, implantable cardioverter-defibrillators, and insertable loop recorders. CIED analysis is recommended at autopsy (1,2), but it is rarely performed (3–5). Selective autopsy case reports, case series, and a large study registry have shown the utility of post-mortem CIED interrogation but have been limited to suspected cases of sudden cardiac death (3,6–10). Consequently, the utility of nonselective CIED analysis at autopsy regardless of suspected cause of death remains unknown. We undertook an institutional registry analysis to determine the clinical role of systematic routine CIED removal, software interrogation, and hardware analysis at autopsy.
Over a period of 6 years, from May 19, 2009, to May 18, 2015, all autopsies undertaken at 2 Johns Hopkins University medical institutions in Baltimore, Maryland, (Johns Hopkins Hospital and Johns Hopkins Bayview Medical Center) used a protocol for routine CIED identification and removal. All autopsy subjects identified as having a CIED were included in the Johns Hopkins Post-mortem CIED Registry (“the registry”). The subjects underwent either complete autopsy or limited autopsy with, at minimum, inclusion of the heart and CIED generator. Consent for autopsy was obtained post-mortem from next of kin or legal guardians.
CIED generators were routinely removed by an autopsy technician using recommended precautions (11–13). In particular, a manufacturer-specific bidirectional hex wrench was used for disconnection of the CIED generator header from the attached indwelling leads to avoid cutting leads, which may trigger inappropriate device therapies and false device alerts. The CIED generator was stored at room temperature until it was interrogated with a manufacturer-specific computer programmer by a board-certified clinical cardiac electrophysiologist (S.K.S.). Appropriate battery and lead parameters, alerts, and electrograms were reviewed and cataloged in the registry. Significant clinical and technical alerts were also reviewed and confirmed by a second board-certified clinical cardiac electrophysiologist (J.E.M.).
Significant CIED alerts
Significant clinical alerts included those triggered by sustained atrial or ventricular tachyarrhythmias within 24 h of death or an elevated OptiVol (Medtronic, Minneapolis, Minnesota) fluid index >60 Ohm-days in the weeks before death. An elevated OptiVol fluid index indicates significant thoracic fluid accumulation as determined by elevated intrathoracic impedance measurements, and this software algorithm is nominally activated in most defibrillators manufactured by Medtronic. By contrast, the intrathoracic impedance alert algorithm (CorVue, St. Jude Medical, St. Paul, Minnesota) found in most defibrillators manufactured by St. Jude Medical is not nominally activated. Significant technical alerts included premature battery depletion, evidence of lead malfunction (fracture or insulation breach), or random component failure.
Inaccurate CIED alerts
Inaccurate technical alerts triggered post-mortem as a result of automated algorithms (capture threshold, sensing, impedance testing) and inaccurate clinical alerts caused by false atrial or ventricular tachyarrhythmias derived from artifact detection were not considered significant and were not catalogued.
The CIED device was then submitted to the applicable manufacturer (Medtronic; Boston Scientific, Natick, Massachusetts; St. Jude Medical; or Biotronik, Lake Oswego, Oregon) for detailed technical analysis (guidelines for processing returned products are available from all manufacturers on request). Standardized manufacturer analysis entailed visual and mechanical inspection, software interrogation, and stabilization of the device at 37°C (to mimic in vivo conditions) before electrical bench testing to assess battery status, pacing and shocking capability accurately. If device failure was suspected, then destructive analysis was undertaken to assess for specific component failure.
The attending pathologist undertook visual inspection, anatomic dissection and measurements, microscopic analysis, and, when appropriate, immunohistochemical staining, toxicology, and genetic studies. The attending pathologist was informed of the CIED interrogation results before their adjudication of the cause, mechanism, and time of death on finalization of the autopsy report. For example, if a subject with methicillin-resistant Staphylococcus aureus sepsis syndrome died suddenly and was noted to have bacterial endocarditis at autopsy and ventricular fibrillation on post-mortem implantable cardioverter-defibrillator interrogation corresponding to the time of death, then the cause of death would be “sepsis,” the mechanism would be “bacterial endocarditis,” and the time of death would be ascertained from their documented terminal rhythm, which was “ventricular fibrillation.” The medical record and final autopsy report were reviewed by an electrophysiologist, and the primary findings were cataloged in the registry.
Definition of sudden death
Sudden death and nonsudden death cohorts were assigned on the basis of the medical record according to the World Health Organization definition of sudden death in the 2010 International Classification of Diseases-10th Revision: sudden, unexpected death within 1 h of acute symptom onset (if witnessed) or within 24 h of the last observation at baseline (if unwitnessed) (14,15). As per societal recommendations, if a subject was resuscitated from cardiac arrest, survived on life support for a limited period of time, and died of irreversible brain damage, then the death was classified as sudden (1).
A retrospective cohort analysis was used. Subjects were classified as dying either suddenly or nonsuddenly by history and as having a primary cardiac cause or noncardiac cause of death on the basis of the findings of the final autopsy report. Chi-square analysis with Yates correction when appropriate was used to compare categorical variables. Mean ± SD were calculated for continuous variables. A 2-tailed p value of <0.05 was considered statistically significant.
Study approval for this post-mortem registry analysis was provided by the Johns Hopkins University School of Medicine Institutional Review Board.
In the registry’s initial 6 years, a total of 2,025 autopsies were undertaken at a Johns Hopkins University medical institution (1,739 at Johns Hopkins Hospital and 286 at Johns Hopkins Bayview Medical Center). A total of 84 subjects (4.2% of all autopsies) were identified as having a CIED; all underwent successful removal of the pacemaker (n = 37) or implantable cardioverter-defibrillator (n = 47). The mean age at death was 64.3 ± 16.8 years (range 6 months to 97 years; median age 65 years). The mean time from the known or reasonably estimated time of death (95% of subjects) to autopsy was 26.7 ± 16.1 h. The mean time from autopsy to CIED interrogation was 17.5 ± 13.2 days. The CIEDs analyzed included those of 4 different manufacturers; Medtronic (36 CIEDs), St. Jude Medical (24 CIEDs), Boston Scientific/Guidant (22 CIEDs), and Biotronik (2 CIEDs).
Most deaths (81%) occurred in a health care facility (57 in teaching hospitals, 6 in community hospitals, 5 in nursing homes or rehabilitation centers) rather than at home (16 in total), and most deaths were witnessed (93%). A total of 43 subjects died suddenly (38 witnessed), and 41 subjects had not died suddenly (40 witnessed). The demographic and CIED characteristics are summarized in Table 1.
Overall, 87% of autopsy subjects underwent complete autopsy, and 13% underwent limited autopsy according to the stipulations of their consent. The most common request in limited autopsies was for exclusion of the head.
Causes of death
The reported primary causes of death in the sudden death group were predominantly cardiac (29 of 43) (Figure 1). Acute infectious causes were the second most common (10 of 43) for this cohort, followed by acute hemorrhage (2 of 43) and pulmonary causes (2 of 43).
Conversely, the reported primary causes of death in the nonsudden death group were predominantly infectious (21 of 41) (Figure 1). Cardiac causes were the second most common (11 of 41) for this cohort, followed by intracranial hemorrhage (3 of 41), neurological causes (2 of 41), pulmonary causes (2 of 41), and hepatic failure (2 of 41).
In the sudden death cohort, the terminal cardiac rhythm was available for review in 35 of 38 (92.1%) of those with witnessed sudden death (Figure 2). Documented terminal rhythms included pulseless electrical activity (47.4%), ventricular tachycardia or ventricular fibrillation (36.8%), and bradyarrhythmia or asystole (7.9%).
Sudden death cohort
On post-mortem CIED interrogation, 62.8% of the CIEDs in sudden death subjects, including 21 defibrillators and 6 pacemakers, exhibited significant alerts. No significant alerts were demonstrated in 37.2% of devices in this group, including 4 defibrillators and 12 pacemakers.
There were 27 sudden death subjects with a total of 30 significant alerts (Figure 2). These alerts included 12 sustained ventricular tachycardia/ventricular fibrillation episodes that were successfully terminated either by internal shocks (10 defibrillator subjects) or external shocks (2 defibrillator subjects). The latter 2 subjects had had their defibrillator inactivated in a perioperative setting necessitating external cardioversion during cardiac arrest. Conversely, 12 episodes of ventricular tachycardia/ventricular fibrillation were not terminated. These subjects included 5 pacemaker recipients without defibrillation capability (example shown in Figure 3), 4 defibrillator recipients exhibiting undersensing and hence no appropriate delivery of therapy, 2 defibrillator subjects with unsuccessful final internal shocks (example shown in Figure 4), and 1 untreated defibrillator subject exhibiting sustained ventricular tachycardia in a “monitor zone” below the programmed heart rate cutoff for device therapy.
Additionally, 5 defibrillator subjects (including 3 with successfully treated ventricular tachycardia/ventricular fibrillation) demonstrated alerts in response to an elevated OptiVol fluid index >60 Ohm-days. One pacemaker subject exhibited an atrial mode switch with the accompanying intracardiac electrogram demonstrating probable sinus tachycardia and frequent premature atrial contractions (>150 beats/min) correlating with the postulated onset of cardiogenic shock resulting from acute myocardial infarction.
Nonsudden death cohort
In 19.5% of those dying nonsuddenly, including 8 defibrillator subjects, a significant clinical alert on post-mortem CIED interrogation was exhibited (Figure 2). No significant alerts were present in the remainder of this group, which included 14 defibrillators and 19 pacemakers.
There were 8 nonsudden death subjects with a total of 9 significant alerts. These included 2 sustained ventricular tachycardia/ventricular fibrillation episodes that were successfully terminated by internal shocks and 7 elevated OptiVol fluid index >60 Ohm-days alerts (including 1 subject with successfully treated ventricular tachycardia/ventricular fibrillation).
Overall, 41.7% of CIEDs in all autopsy subjects exhibited a significant clinical alert within 24 hours of death (6 pacemakers, 29 defibrillators), whereas 58.3% did not (31 pacemakers, 18 defibrillators). A much greater likelihood of a significant clinical alert was observed in those CIED subjects with sudden death (27 of 43) compared with those CIED subjects with nonsudden death (8 of 41; chi-square = 14.50; p < 0.001) (Central Illustration). In particular, clinical alerts in response to ventricular tachycardia/ventricular fibrillation episodes were significantly more common in the sudden death cohort (24 of 43) as compared with the nonsudden death cohort (2 of 41; chi-square = 23.15; p < 0.001).
When considering CIED type (defibrillator vs. pacemaker), there was a much greater likelihood of a significant clinical alert in defibrillator recipients (29 of 47) than in pacemaker recipients (6 of 37; chi-square = 15.81; p < 0.001). Clinical alerts in response to ventricular tachycardia/ventricular fibrillation episodes were significantly more likely in defibrillator recipients (21 of 47) compared with pacemaker recipients (5 of 37; chi-square = 8.00; p < 0.005).
Additionally, comparison was made of CIED alerts in those subjects assigned a primary cardiac cause of death (27 of 40 had alerts) versus those with a primary noncardiac cause of death (8 of 44 had alerts). This finding demonstrated a much greater likelihood of a significant clinical alert noted in those subjects judged to have a cardiac rather than a noncardiac primary cause of death (chi-square = 18.97; p < 0.001). Alerts specifically related to ventricular tachycardia/ventricular fibrillation were significantly more likely in subjects deemed to have a cardiac cause of death (21 of 40) compared with subjects deemed to have a noncardiac cause of death (5 of 44; chi-square = 14.72; p < 0.001). For an example of a patient with a cardiac cause of death but without an evident CIED alert on interrogation, see Figure 5.
Manufacturer analyses revealed occult premature battery depletion in 1 pacemaker that had been subject to a U.S. Food and Drug Administration (FDA) class II recall. An abnormality in battery status had not been evident on routine post-mortem interrogation but was revealed after detailed technical analysis by the manufacturer. In addition, manufacturer analysis also uncovered a case of hard reset (nonprogrammable software) caused by cold exposure (from device refrigeration) post-mortem and not by component failure. Overall, detailed technical hardware analyses revealed no cases of CIED component failure contributing to death.
Fluid index alerts
Of the 84 CIEDs examined post-mortem, 21 were implantable cardioverter-defibrillators manufactured by Medtronic. A total of 17 of these 21 defibrillators were equipped with Medtronic OptiVol fluid index monitoring software. This algorithm begins deriving values 34 days post-implantation. Overall, 2 subjects did not have fluid index monitoring values available because they were <34 days post-CIED implantation, 3 subjects displayed normative values (<60 Ohm-days), and 12 subjects displayed an alert in response to a fluid index value >60 Ohm-days at the time of death. Autopsy findings in all 12 subjects with an OptiVol fluid index alert triggered by a value >60 Ohm-days correlated with significant respiratory disease. These findings included decompensated congestive heart failure as evidenced by pulmonary congestion (n = 8), pneumonia (n = 1), pneumonia and diffuse alveolar damage (n = 1), aspiration (n = 1), and a large left-sided pleural effusion with pulmonary embolism (n = 1). Similarly, the 3 subjects without an OptiVol fluid index alert also had significant respiratory disease, including decompensated congestive heart failure (n = 2) and pneumonia and diffuse alveolar damage (n = 1). Hence the fluid index alert (OptiVol) had a sensitivity of 80% with a specificity of 67% for congestive heart failure in our autopsy population. None of the 5 defibrillators equipped with the intrathoracic impedance alert algorithm (CorVue) had the algorithm activated.
In the United States, CIEDs are present in 4% or 8% of autopsy subjects who have died out of hospital or in hospital, respectively (10,16). However, at autopsy these devices have historically been viewed as nonrelevant passive implants rather than accessible sources of computerized clinical information to help adjudicate significant clinical events. For example, from 2001 to 2007, a total of 31,733 autopsies were undertaken by the Los Angeles County Department of the Coroner, but only 20 subjects (0.06%) were selected for additional CIED analysis (3). Conversely, 2 retrospective post-mortem pacemaker analyses (9,17) undertaken in Europe identified frequent sustained ventricular tachyarrhythmias and device abnormalities, respectively. However, most of the aforementioned study subjects did not undergo an autopsy investigation, and this limitation made the importance of their post-mortem CIED findings difficult to place in full clinical perspective.
In 2007, the Association for European Cardiovascular Pathology issued guidelines, published in 2008 (1), that recommended CIED removal and interrogation at autopsy when investigating cases of potential sudden cardiac death. This approach was recently validated in the prospective POST SCD (Post-mortem Systematic Investigation of Sudden Cardiac Death) study examining 22 CIED carriers among 517 reported out-of-hospital sudden deaths in San Francisco, California (10). However, the clinical utility of routine CIED analysis at all autopsy investigations was not addressed. In this regard, our institutional registry represents a large post-mortem CIED study of autopsy subjects and one that used a nonselective systematic approach to CIED removal and analysis. It revealed significant clinical findings in 62.8% of sudden death cases and in 19.5% of nonsudden death cases, thus assisting in the determination of timing, mechanism, and cause of death. The likelihood of detecting significant CIED alerts was noted to be higher in cases of sudden death as compared with nonsudden death, defibrillator recipients as compared with pacemaker recipients, and those with a cardiac cause of death as compared with a noncardiac cause of death. However, given the significant yield of clinical alerts in subjects with cardiac and noncardiac sudden death and in almost 20% of those subjects judged to have died nonsuddenly, we propose that pathologists and medical examiners undertake CIED removal and analysis in all subjects undergoing autopsy investigation.
In our sudden death cohort, of which 72% had died in a health care facility, the predominant terminal rhythm was pulseless electrical activity (47.4%), which is consistent with previous studies of in-hospital sudden death and contrasts with the predominant terminal rhythm of ventricular tachycardia/ventricular fibrillation (59%) seen in the aforementioned out-of-hospital POST SCD study (10).
The OptiVol fluid index values are derived from alterations in intrathoracic impedance measurements (between the lead in the right ventricle and the defibrillator generator). These values have been shown to correlate with elevated pulmonary capillary wedge pressure as a result of fluid accumulation in the lungs and thus indicate decompensated congestive heart failure (18,19). Clinical studies have shown a sensitivity of 60% to 80% in correlating an OptiVol fluid index alert of >60 Ohm-days for decompensated congestive heart failure (20–23). We observed an elevated OptiVol fluid index alert >60 Ohm-days in 12 of 17 subjects equipped with this Medtronic software program, which is routinely activated on defibrillator implantation. At autopsy, we observed that the OptiVol fluid index alert had a sensitivity of 80% and a specificity of 67% for congestive heart failure. The 33% of subjects demonstrating a “false-positive” alert nevertheless had relevant noncardiac respiratory disease (aspiration, pneumonia, pleural effusion, and pulmonary embolism), suggesting a high specificity for significant cardiorespiratory disease in general. Only 25% of autopsy subjects had a defibrillator equipped with the OptiVol fluid index alert algorithm, which is designed to reflect thoracic fluid accumulation over a period of weeks rather than <24 h. Accordingly, when nonarrhythmic alerts were excluded, the yield of CIED alerts on post-mortem analysis was reduced to 58.1% (25 of 43) in sudden death subjects and 4.9% (2 of 41) of subjects in the nonsudden death group.
Currently, the bulk of post-marketing surveillance data collected by manufacturers, as mandated by the U.S. FDA, is obtained from CIEDs returned from stable patients undergoing elective operations to replace or upgrade their existing CIED systems, rather than from patients who have died. In fact, a contemporary survey of 71 Chicago metropolitan area morticians indicated that only 4% of them return CIEDs to the manufacturer, whereas 44% of morticians discard CIEDs as medical waste (4). This practice is unfortunate because major defibrillator and pacemaker generator as well as defibrillator lead recalls in the last decade highlight the ongoing need for pursuing both software interrogation and hardware analysis in patients who have died, to determine more accurately the true incidence of potentially fatal CIED component failure. In our post-mortem population, manufacturer analyses ruled out CIED malfunction in a case of software hard reset, and they accurately detected a case of nonfatal premature pacemaker battery depletion in a device that was subject to a U.S. FDA class II recall. Furthermore, in 7 subjects with defibrillators and documented ventricular tachycardia/ventricular fibrillation, we noted 4 cases of ventricular undersensing, 2 cases with unsuccessful final internal shocks, and 1 case of withheld therapy as a result of a programmed heart rate cutoff for therapy set above the rate of the ventricular arrhythmia. Such instances raise potential concerns regarding implantable cardioverter-defibrillator programming and device performance. Hence we would advocate that other academic medical centers and medical examiner facilities adopt a similar approach to help clinicians and manufacturers accurately ascertain cases of both nonfatal and fatal CIED failure.
Inherent to all autopsy studies is the selection bias that occurs when choosing which subjects are to undergo investigation because this can produce a population with an elevated rate of significant findings. Fortunately, our study included not only autopsy subjects studied for clinical indications (sudden death) but also subjects studied for altruistic purposes (enrollment in a longitudinal research study or an unexplained illness associated with nonsudden death). We believe that our nonselective approach to CIED removal and analysis in all autopsy subjects regardless of whether death was deemed sudden or nonsudden allowed us to avoid selection bias toward sudden cardiac death. Nevertheless, in contrast to our study, more than 90% of sudden cardiac deaths occur out of hospital (24). Thus, our study likely overestimates the incidence of pulseless electrical activity and underestimates the incidence of ventricular tachycardia/ventricular fibrillation as a terminal rhythm in the larger population with CIEDs.
A second major limitation stems from the issue that the CIED alerts examined can be viewed only for their association with the timing, mechanism, and cause of death and not as evidence of direct causation. Hence we would caution against pursuing CIED removal and analysis in isolation but rather recommend that it be undertaken as part of an autopsy investigation to ensure a complete clinical context. Additionally, most subjects were not followed at our institution, and therefore we were unable to address systematically whether ante-mortem arrhythmias or transthoracic impedance changes contributed to subjects’ outcomes.
Finally, a third limitation is the inclusion of 4 different CIED manufacturers in our study. There are variations in each CIED manufacturer’s software programming and nominal parameters for alert detections, so it is possible that a similar study with a different composition of CIED types and manufacturers could have some differences in their results related to CIED heterogeneity.
Given the clinical data observed in our institutional registry, we would recommend CIED removal and analysis in all subjects undergoing autopsy investigation to assist in the determination of timing, mechanism, and cause of death. We would also support recent calls (4,5,13) for mandatory post-mortem CIED retrieval and manufacturer analysis to screen for potentially fatal device malfunction more accurately.
COMPETENCY IN MEDICAL KNOWLEDGE: Post-mortem analysis of CIEDs can yield important diagnostic information and identify instances of device failure.
COMPETENCY IN SYSTEMS-BASED PRACTICE: Hospitals and medical examiner facilities performing autopsies should follow protocols that ensure identification, safe removal, and timely interrogation of CIEDs.
TRANSLATIONAL OUTLOOK: Wider adoption of post-mortem CIED analysis at a large number of medical institutions could provide expanded post-marketing surveillance data and lead to improved device design and programming.
Dr. Rickard has reported consulting for Medtronic. Dr. Cheng is currently an employee of Medtronic. All other authors have reported that they have no relationships relevant to the contents of this paper to disclose.
- Abbreviations and Acronyms
- cardiovascular implantable electronic device
- Food and Drug Administration
- Received May 4, 2016.
- Revision received June 14, 2016.
- Accepted June 14, 2016.
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