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Review |

Changes in Rates of Autopsy-Detected Diagnostic Errors Over Time:  A Systematic Review FREE

Kaveh G. Shojania, MD; Elizabeth C. Burton, MD; Kathryn M. McDonald, MM; Lee Goldman, MD, MPH
[+] Author Affiliations

Author Affiliations: Department of Medicine, University of California, San Francisco (Drs Shojania and Goldman); Department of Pathology and Laboratory Medicine, Baylor Health Care System, Dallas-Fort Worth, Tex (Dr Burton); and Center for Primary Care and Outcomes Research, Stanford University, Stanford, Calif (Ms McDonald).


JAMA. 2003;289(21):2849-2856. doi:10.1001/jama.289.21.2849.
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Context Substantial discrepanies exist between clinical diagnoses and findings at autopsy. Autopsy may be used as a tool for quality management to analyze diagnostic discrepanies.

Objective To determine the rate at which autopsies detect important, clinically missed diagnoses, and the extent to which this rate has changed over time.

Data Sources A systematic literature search for English-language articles available on MEDLINE from 1966 to April 2002, using the search terms autopsy, postmortem changes, post-mortem, postmortem, necropsy, and posthumous, identified 45 studies reporting 53 distinct autopsy series meeting prospectively defined criteria. Reference lists were reviewed to identify additional studies, and the final bibliography was distributed to experts in the field to identify missing or unpublished studies.

Study Selection Included studies reported clinically missed diagnoses involving a primary cause of death (major errors), with the most serious being those likely to have affected patient outcome (class I errors).

Data Extraction Logistic regression was performed using data from 53 distinct autopsy series over a 40-year period and adjusting for the effects of changes in autopsy rates, country, case mix (general autopsies; adult medical; adult intensive care; adult or pediatric surgery; general pediatrics or pediatric inpatients; neonatal or pediatric intensive care; and other autopsy), and important methodological features of the primary studies.

Data Synthesis Of 53 autopsy series identified, 42 reported major errors and 37 reported class I errors. Twenty-six autopsy series reported both major and class I error rates. The median error rate was 23.5% (range, 4.1%-49.8%) for major errors and 9.0% (range, 0%-20.7%) for class I errors. Analyses of diagnostic error rates adjusting for the effects of case mix, country, and autopsy rate yielded relative decreases per decade of 19.4% (95% confidence interval [CI], 1.8%-33.8%) for major errors and 33.4% (95% [CI], 8.4%-51.6%) for class I errors. Despite these decreases, we estimated that a contemporary US institution (based on autopsy rates ranging from 100% [the extrapolated extreme at which clinical selection is eliminated] to 5% [roughly the national average]), could observe a major error rate from 8.4% to 24.4% and a class I error rate from 4.1% to 6.7%.

Conclusion The possibility that a given autopsy will reveal important unsuspected diagnoses has decreased over time, but remains sufficiently high that encouraging ongoing use of the autopsy appears warranted.

Figures in this Article

Beginning in 19121 and continuing to 2002,26 researchers have documented substantial discrepancies between clinical diagnoses and findings at autopsy. Time series from single institutions have examined trends in these diagnostic discrepancies and, with only 1 exception,7 have found no significant decreases over time.812

A possible explanation for the stability of these rates is increased selection by clinicians. In 1994, the last year for which national data exist, the autopsy rate for all nonforensic deaths decreased to less than 6%13 compared with average rates of 30% to 40% in the 1960s.14 With progressively fewer autopsies performed over time, clinical selection for diagnostically challenging cases might offset true gains in diagnostic accuracy. However, several prospective studies have shown clinicians to have little ability to identify cases that will yield "diagnostic surprises,"1518 so clinical selection might exert little effect on rates of autopsy-detected diagnostic errors.

As part of a broader report on the autopsy as a tool for quality measurement and improvement,19 we systematically reviewed the literature to estimate the frequency with which autopsy reveals important, clinically missed diagnoses. We sought to assess the degree to which this frequency has changed over time, and the extent to which clinical selection for diagnostically challenging cases accounts for the substantial error rates that continue to be reported in autopsy studies.

Search Strategy

We searched the MEDLINE database for English-language articles (1966-April 2002) using Medical Subject Heading terms autopsy and postmortem changes, and the title words, autopsy, post-mortem, postmortem, necropsy, and posthumous. We then applied terms capturing aspects of study design (eg, epidemiologic studies, clinical trials) and topics relating to diagnosis (eg, diagnostic errors, diagnostic techniques and procedures) or error (eg, medical error, iatrogenic disease, safety). Reference lists from all relevant articles were reviewed to identify additional studies, and the final bibliography was distributed to experts in the field to identify missing or unpublished studies.

Study Selection

Included studies met the following criteria:

1. Consecutive autopsies with well-defined selection criteria (eg, all adults dying after hospital arrival and undergoing autopsy during a specified period) or random samples from such series; "convenience samples" and consecutive series missing more than 20% of eligible cases were excluded.

2. Clinical diagnoses derived from autopsy request forms submitted by clinicians or chart review performed by study investigators; assessments of clinical diagnoses based primarily on death certificates were excluded.

3. Classification of autopsy-detected errors in clinical diagnoses according to generally accepted classification schemes8,20; major errors defined as clinically missed diagnoses involving a principal underlying disease or primary cause of death; and class I errors, major errors that, had they been detected during life, "would," "could," "possibly," or "might" have affected patient prognosis or outcome (at a minimum, discharge from the hospital alive). Studies that made no distinction between changes in management and changes in outcome were deemed to be reporting major errors only.

Studies reporting autopsy data from multiple institutions or observation periods were analyzed as separate series whenever possible. We did not restrict our review to studies of inhospital deaths, although an overwhelming majority of studies involved inpatient autopsies predominantly or, in many cases, exclusively.

Quantitative Analysis

Diagnostic error rates were modeled using logistic regression analyses with country, study period, case mix, and autopsy rate as predictors and including a random study effect.21 Hospital teaching status was not included as a predictor, because too few studies involved nonteaching hospitals and because the nature of the teaching status was often unclear.

Autopsy rates and time were modeled as continuous variables, with the value for time designated as the midpoint of the study period. Country was simplified to United States or non-United States, but case mix was modeled as a nonordinal variable with the categories of (1) general autopsies, (2) adult medical, (3) adult intensive care, (4) adult or pediatric surgery, (5) general pediatrics or pediatric inpatients, (6) neonatal or pediatric intensive care, and (7) other. The first category, which constituted the base case mix in the regression analysis, included series reporting general autopsies (all ages, specialties, and settings), general inpatients (all ages and specialties), and general adult inpatients. We combined these 3 populations because many studies provided insufficient detail to permit reliable distinctions between these 3 and because the contribution of adult inpatients dominated samples of all 3 types.

In anticipation of methodological heterogeneity among the studies, we abstracted each article for key study features plausibly related to observed error rates. These study features included (1) cohort design (prospective vs retrospective); (2) clarity of error definition (whether class I and major errors were defined using illustrative examples or if the results included a complete listing of all clinical-autopsy discrepancies designated as class I or major errors); (3) source of clinical diagnoses (chart review vs autopsy request forms); (4) involvement of clinicians in classifying errors. The regression models for major and class I error rates incorporated each of these methodological characteristics as categorical variables.

Included Autopsy Series

We identified 45 studies28,12,17,18,20,2255 reporting a total of 53 distinct autopsy series meeting our inclusion criteria (Table 1a). More studies reported major errors than reported class I errors (42 and 37 series, respectively). Twenty-six series reported both types of errors and just over half of the series (27) involved US institutions.

Table Graphic Jump LocationTable 1a. Major or Class I Error Rates of Autopsy Series Between 1959 and 1999

Although numerous studies met our inclusion criteria and offered a wide range of predictor variables for the regression model (Table 2), many of the studies exhibited methodological limitations. The vast majority of autopsy series were assembled retrospectively, and only half performed chart review to obtain clinical diagnoses. Clinicians played a primary role in classifying diagnostic errors in two thirds of series (Table 3).

Table Graphic Jump LocationTable 2. Demographic Features of Included Autopsy Series*
Table Graphic Jump LocationTable 3. Methodological Features of Included Autopsy Series
Diagnostic Error Rates

The median major error rate was 23.5%, although rates ranged from 4.1% to 49.8%, with the upper bound reflecting the only series focused on postoperative deaths.44 The median class I error rate was 9.0%, but rates ranged from 0% to 20.7%, with the upper bound again corresponding to the series focused on postoperative deaths.44 The study reporting zero class I errors involved pediatric deaths from an emergency department.49 The authors attributed the absence of class I errors to the high proportion of deaths following cardiac arrest, in which survival depends predominantly on the adequacy of resuscitation rather than the accuracy of clinical diagnosis.

Effects of Country, Autopsy Rates, and Case Mix

Compared to US studies, autopsy series from outside the United States exhibited a slight, but statistically significant trend toward higher major error rates (odds ratio [OR], 1.15; 95% confidence interval [CI], 1.01-1.31; P = .03). For class I errors, the effect was of comparable magnitude and bordered on statistical significance (OR, 1.26; 95% CI, 0.99-1.59; P = .06) (Table 4).

Table Graphic Jump LocationTable 4. Effects of Various Study Characteristics on Diagnostic Error Rates

Autopsy rates ranged from 12% to 100% (median, 37.0%). Relative to the error rate in 1980 (the midpoint of the 40-year period spanned by the included studies), major errors decreased at a rate of 12.4% (95% CI, 7.0%-17.6%) for every 10% increase in autopsy rates. Class I errors decreased at a rate of 17.4% (95% CI, 6.6%-27.1%) for every 10% increase in autopsies.

Autopsy series restricted to surgical patients reported significantly higher rates of both major errors (OR, 2.16; 95% CI, 1.53-3.06) and class I errors (OR, 3.01; 95% CI, 1.66-5.43). Series limited to adult medical patients reported higher class I error rates (OR, 1.84; 95% CI, 1.06-3.20); US series from adult intensive care units also had higher class I error rates (OR, 2.12; 95% CI, 1.42-3.16). Conversely, pediatric series reported significantly lower rates of major errors, and series involving pediatric or neonatal intensive care autopsies reported significantly lower class I error rates (OR, 0.56; 95% CI, 0.32-0.98) (Table 4).

Impact of Methodological Features

None of the 4 methodological features shown in Table 3 significantly affected major error rates, but 2 methodological features significantly affected class I error rates (Table 4). Studies conducted prospectively reported higher class I error rates (OR, 1.63; 95% CI, 1.19-2.23), as did studies in which clinicians played active roles in classifying errors (OR, 2.09; 95% CI, 1.31-3.34).

Trends in Diagnostic Errors Over Time

Adjusting for the effects of country, case mix, and autopsy rates, major errors significantly decreased over time, with a relative reduction of 19.4% per decade (95% CI, 1.8%-33.8%). Adjusting for these same factors as well as the 2 significant methodological features (prospective study design and clinicians participation in classifying errors), class I error rates also decreased significantly over time, with a relative reduction of 33.4% per decade (95% CI, 8.4%-51.6%).

Despite these decreases, we estimated that a contemporary US institution with an autopsy rate of 5% (roughly the national average13), could observe a major error rate of 24.4% (95% CI, 18.8%-31.1%) and a class I error rate of 6.7% (95% CI, 3.8%-11.4%) (Figure 1 and Figure 2, respectively). With an autopsy rate of 37% (the median rate in the included studies), major and class I error rates in the same institution would be estimated as 17.4% (Figure 1) and 5.8% (Figure 2). This autopsy rate is much higher than the rates of 15% to 20% typically achieved in contemporary teaching hospitals56 and, therefore, has less clinical selection. Even with extrapolation to an autopsy rate of 100% (to eliminate the effect of clinical selection completely), a US institution in 2000 would be estimated to report a major error rate of 8.4% (95% CI, 5.2%-13.1%) and a class I error rate of 4.1% (95% CI, 1.6%-9.9%) (Figure 1 and Figure 2, respectively).

Figure 1. Major Error Rates
Graphic Jump Location
Major error rates were generated from the regression model, setting country to United States and using 3 different autopsy rates: 5% (roughly the national average13), 37% (the median rate in the included studies), and 100%. Extrapolation to an autopsy rate of 100% minimizes the effect of clinical selection and thus provides a lower bound for the major error rate.
Figure 2. Class I Error Rates
Graphic Jump Location
Class I error rates were generated from the regression model, setting country to United States and using 3 different autopsy rates: 5% (roughly the national average13), 37% (the median rate in the included studies) and 100%. Extrapolation to an autopsy rate of 100% minimizes the effect of clinical selection and thus provides a lower bound for the class I error rate. Adjusting for the effects of study design (prospective vs retrospective) and clinician involvement in classifying errors significantly impacts estimates from earlier periods, but the adjusted and unadjusted estimates converge over time. For 2000, estimated class I error rates are virtually identical regardless of primary study design and clinician involvement in classifying errors.

By analyzing the results of 53 distinct autopsy series over a 40-year period, we have shown statistically significant decreases over time for major and class I diagnostic errors detected at autopsy. By contrast, individual studies comparing rates of autopsy-detected diagnostic errors from different periods have found strikingly unchanged error rates.8,12,57,58 These previous results almost certainly reflect inadequate power, as well as the competing effects of improvements over time and increased clinical selection as autopsy rates decrease. In fact, the only study with high and nearly equal autopsy rates in all periods examined showed a significant decrease in major errors over time.7

The present data suggest that, among the approximately 850 000 individuals dying in US hospitals each year,59,60 a major diagnosis remains clinically undetected in at least 8.4% of cases (71 400 deaths). The data also suggest that approximately 34 850 of these patients might have survived to discharge had misdiagnosis not occurred, but this estimate depends on the accuracy of the designator of class I error. Although, this second number is more speculative, given the dependence of class I error estimates on methodological features of the primary studies, it can be considered in the context of the Institute of Medicine's estimates of 44 000 to 98 000 preventable deaths per year due to medical error.61 These latter estimates have been debated,6264 but the studies from which they were derived may not have detected many of the errors reported in our analysis.

A major limitation of any systematic review is the possibility of publication bias. Problems with existing methods of assessing publication bias65,66 are compounded by the opposing directions in which publication bias might operate. Lack of interest might result in fewer published reports of low error rates, whereas self-censorship might reduce reports of high error rates. Regardless of the true net effect of publication bias on autopsy studies, if this effect has remained reasonably stable, the observed decrease in published error rates over time would still be meaningful.

Only 5 studies7,31,39,41,52 addressed the issue of reproducibility for the classification of autopsy-detected diagnostic errors, and none provided sufficient detail to permit calculation of formal measures of agreement. The issue of reproducibility is particularly important for class I errors, as no study used validated criteria to guide reviewers' judgments about affects on prognosis, which are known to exhibit substantial variability.62

Even more fundamental than reproducibility of the error classifications is the question of the autopsy's characteristics as a diagnostic test. Determining the sensitivity of any criterion standard, including the autopsy, presents difficulties. As reviewed in greater detail elsewhere,19 technically adequate autopsies fail to establish the cause of death in 1% to 5% of cases, although some studies have reported substantially higher rates of persistent diagnostic uncertainty after autopsy,43 especially in perinatal deaths.6769

Only 1 study70 has assessed agreement among pathologists in determining principal underlying diseases and causes of death. Four pathologists independently reviewing 35 autopsies reported excellent to near perfect agreement for determining the principal disease (ie, underlying cause of death), with κ values between 0.83 and 0.97 for the different pathologist pairs. For assignments of the immediate cause of death, however, the pathologists exhibited only moderate to substantial agreement (κ values ranging from 0.43-0.75).

We used the term error throughout our analysis because of its ubiquitous presence in the autopsy literature. However, it remains unclear to what extent clinically missed diagnoses represent errors per se, rather than acceptable limits of antemortem diagnosis in the face of atypical clinical presentations. In fact, because the vast majority of autopsy studies come from teaching hospitals, published autopsy series may be enriched for atypical cases. Nonetheless, the autopsy has historically helped define how cases that previously appeared atypical could more commonly be recognized antemortem. Repeated detection of certain missed diagnoses may result in the recognition that some patterns of presentation are more typical than previously appreciated.

For many physicians, interest in the autopsy as a means of detecting clinically missed diagnoses is undoubtedly offset by concerns over litigation. Only 1 study34 explicitly addressed the question of whether autopsy findings influence malpractice claims. In this series of 176 autopsies from the University of Pittsburgh Medical Center (Pittsburgh, Pa) in 1994, follow-up of all cases after the statute of limitations on malpractice suits had expired identified only 1 malpractice suit. Review of the hospital record indicated that the intent to proceed to litigation in that case had become clear prior to the patient's death.

In addition to their intrinsic clinical interest, missed diagnoses detected at autopsy may have important implications for research. Health services researchers are accustomed to the problem that administrative databases contain systematic errors and biases compared with the medical record.7173 The data presented here indicate that the medical record itself contains substantial inaccuracies regarding the principal diagnoses causing or contributing to death. Since principal diagnoses and causes of death are determined without autopsy in the vast majority of cases, vital statistics, clinical registries, and even randomized trials capture incorrect causes of death at rates comparable with the major error rates in our analysis. These inaccuracies have important policy implications, as major funding and policy decisions derive in part from vital statistics and other estimates of disease burden.7476

Correcting such inaccuracies would not require substantial increases in autopsies at all hospitals. Perhaps a small group of hospitals funded to perform autopsies in a high percentage of deaths and according to a uniform protocol could generate accurate error rates appropriate for correcting the information contained in routinely generated death certificates and other epidemiological databases. Data from such a program would also provide the opportunity to develop an approach to enhancing the selection of autopsies likely to reveal important unsuspected diagnoses. Explicit selection of autopsy cases on the basis of diagnostic uncertainty would represent an advance over current autopsy selection, which is likely determined in large part by patients' demographic characteristics (especially age7779) and by clinicians' comfort in requesting autopsy.80,81 Most importantly, further research conducted in centers with high autopsy rates would permit development of strategies for using autopsy findings to improve subsequent clinical performance.

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Meier PR, Manchester DK, Shikes RH, Clewell WH, Stewart M. Perinatal autopsy: its clinical value.  Obstet Gynecol.1986;67:349-351.
Hagerstrand I, Lundberg LM. The importance of post-mortem examinations of abortions and perinatal deaths.  Qual Assur Health Care.1993;5:295-297.
Saller Jr DN, Lesser KB, Harrel U, Rogers BB, Oyer CE. The clinical utility of the perinatal autopsy.  JAMA.1995;273:663-665.
Veress B, Gadaleanu V, Nennesmo I, Wikstrom BM. The reliability of autopsy diagnostics: inter-observer variation between pathologists, a preliminary report.  Qual Assur Health Care.1993;5:333-337.
Green J, Wintfeld N. How accurate are hospital discharge data for evaluating effectiveness of care?  Med Care.1993;31:719-731.
Malenka DJ, McLerran D, Roos N, Fisher ES, Wennberg JE. Using administrative data to describe casemix: a comparison with the medical record.  J Clin Epidemiol.1994;47:1027-1032.
Romano PS. Can administrative data be used to compare the quality of health care?  Med Care Rev.1993;50:451-477.
Gross CP, Anderson GF, Powe NR. The relation between funding by the National Institutes of Health and the burden of disease.  N Engl J Med.1999;340:1881-1887.
Varmus H. Evaluating the burden of disease and spending the research dollars of the National Institutes of Health.  N Engl J Med.1999;340:1914-1915.
Lamarre-Cliche M, Castilloux AM, LeLorier J. Association between the burden of disease and research funding by the Medical Research Council of Canada and the National Institutes of Health: a cross-sectional study.  Clin Invest Med.2001;24:83-89.
Davis CJ. Autopsy rates: the decline with age.  PAS Rep.1979;16:31-41.
Ahronheim JC, Bernholc AS, Clark WD. Age trends in autopsy rates: striking decline in late life.  JAMA.1983;250:1182-1186.
Sinard JH. Factors affecting autopsy rates, autopsy request rates, and autopsy findings at a large academic medical center.  Exp Mol Pathol.2001;70:333-343.
Rosenbaum GE, Burns J, Johnson J, Mitchell C, Robinson M, Truog RD. Autopsy consent practice at US teaching hospitals: results of a national survey.  Arch Intern Med.2000;160:374-380.
Sanner MA. Medical students' attitudes toward autopsy: how does experience with autopsies influence opinion?  Arch Pathol Lab Med.1995;119:851-858.

Figures

Figure 1. Major Error Rates
Graphic Jump Location
Major error rates were generated from the regression model, setting country to United States and using 3 different autopsy rates: 5% (roughly the national average13), 37% (the median rate in the included studies), and 100%. Extrapolation to an autopsy rate of 100% minimizes the effect of clinical selection and thus provides a lower bound for the major error rate.
Figure 2. Class I Error Rates
Graphic Jump Location
Class I error rates were generated from the regression model, setting country to United States and using 3 different autopsy rates: 5% (roughly the national average13), 37% (the median rate in the included studies) and 100%. Extrapolation to an autopsy rate of 100% minimizes the effect of clinical selection and thus provides a lower bound for the class I error rate. Adjusting for the effects of study design (prospective vs retrospective) and clinician involvement in classifying errors significantly impacts estimates from earlier periods, but the adjusted and unadjusted estimates converge over time. For 2000, estimated class I error rates are virtually identical regardless of primary study design and clinician involvement in classifying errors.

Tables

Table Graphic Jump LocationTable 1a. Major or Class I Error Rates of Autopsy Series Between 1959 and 1999
Table Graphic Jump LocationTable 2. Demographic Features of Included Autopsy Series*
Table Graphic Jump LocationTable 3. Methodological Features of Included Autopsy Series
Table Graphic Jump LocationTable 4. Effects of Various Study Characteristics on Diagnostic Error Rates

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Saller Jr DN, Lesser KB, Harrel U, Rogers BB, Oyer CE. The clinical utility of the perinatal autopsy.  JAMA.1995;273:663-665.
Veress B, Gadaleanu V, Nennesmo I, Wikstrom BM. The reliability of autopsy diagnostics: inter-observer variation between pathologists, a preliminary report.  Qual Assur Health Care.1993;5:333-337.
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Malenka DJ, McLerran D, Roos N, Fisher ES, Wennberg JE. Using administrative data to describe casemix: a comparison with the medical record.  J Clin Epidemiol.1994;47:1027-1032.
Romano PS. Can administrative data be used to compare the quality of health care?  Med Care Rev.1993;50:451-477.
Gross CP, Anderson GF, Powe NR. The relation between funding by the National Institutes of Health and the burden of disease.  N Engl J Med.1999;340:1881-1887.
Varmus H. Evaluating the burden of disease and spending the research dollars of the National Institutes of Health.  N Engl J Med.1999;340:1914-1915.
Lamarre-Cliche M, Castilloux AM, LeLorier J. Association between the burden of disease and research funding by the Medical Research Council of Canada and the National Institutes of Health: a cross-sectional study.  Clin Invest Med.2001;24:83-89.
Davis CJ. Autopsy rates: the decline with age.  PAS Rep.1979;16:31-41.
Ahronheim JC, Bernholc AS, Clark WD. Age trends in autopsy rates: striking decline in late life.  JAMA.1983;250:1182-1186.
Sinard JH. Factors affecting autopsy rates, autopsy request rates, and autopsy findings at a large academic medical center.  Exp Mol Pathol.2001;70:333-343.
Rosenbaum GE, Burns J, Johnson J, Mitchell C, Robinson M, Truog RD. Autopsy consent practice at US teaching hospitals: results of a national survey.  Arch Intern Med.2000;160:374-380.
Sanner MA. Medical students' attitudes toward autopsy: how does experience with autopsies influence opinion?  Arch Pathol Lab Med.1995;119:851-858.

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