American Journal of Industrial Medicine 22:46!M80 (1992)

ARTICLES

Use of Death Certificates in Epidemiological Studies, Including Occupational Hazards: Discordance With Clinical and Autopsy Findings Irving J. Selikoff*, MD

There has long been evidence of frequent inaccuracy of death certificates, with significant discordance between such designations and clinical and autopsy data. This exists for occupational diseases as well. The use of statistical rates based on death certificates has been seriously questioned despite their utility for total mortality. Programs to supplement death certificate data, particularly in occupational disease studies, may be helpful, and are reviewed. o 1992 Wiley-Liss, Inc. Key words: death certificate inaccuracies, occupational mortality studies, statistical rates

INTRODUCTION

There has been evidence that categorizations of causes of death on death certificates are frequently incorrect, in some circumstances 20-40% of reported listings. This has led a number of scientists to question whether they should be used to either establish expected frequencies of the spectrum of diseases or to serve for comparison with groups whose mortality experiences are being investigated. Occasionally, such disagreement and dissatisfaction have been vigorously put. Briggs [1975], reviewing findings in a personal series of 260 autopsies, concluded that “U.S.vital statistics on causes of death bear little relation to the actual state of affairs.” Gittelsohn and Senning [ 19791 were in general agreement, considering that mortality statistics were of “dubious accuracy” because of differences between death certificates and clinical and autopsy records. Glasser [1981] in an editorial in the American Journal of Public Health found that neither accuracy nor interpretation of a study of the question were “very heartening” and Carter [1985] noted that since the landmark paper by Wells in 1923, over 100 publications had documented discrepancies ranging from 20% to 40% with major clinical and autopsy diagnoses and concluded that “Reliance on the diagnosis listed on death certificates will continue to lead to inaccurate statistics on the incidence and nature of lethal disease processes.” *Dr. Selikoff died on May 20, 1992. Mount Sinai School of Medicine of the City University of New York, New York, NY. Address reprint requests to Dr. Stephen Levin, Mount Sinai School of Medicine, One Gustave L. Levy Place, Box 1059, New York, NY 10029. Accepted for publication January 8, 1992. 0 1992 Wiley-Liss, Inc.

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Feinstein and his colleagues [1989] have been perhaps most outspoken on the matter, and believe that there is no scientific justification for calculating incidence from what they consider the grossly inaccurate data that appear on death certificates. While the custom may have been accepted for most of this century, “it now has the same scientific validity as archaic old ideas about alchemy.” REPORTS OF INVESTIGATIONS

There have been inadequacies in a number of important areas, which have led to the dissatisfication expressed in the foregoing. The investigation which initiated questioning of the accuracy of death certificates was that of Wells [1923]. He reviewed 2,712 autopsies at the Cook County Hospital in Chicago and addded 1,OOO of his own. There were 525 cases of malignant disease of which 32.66% had not been so recognized; there were also 23 “cancers” negative at necropsy. Disappointed, Wells concluded that his study showed ‘‘emphatically the lack of value of all recorded vital statistics on cancer . , . we have at the present time no reliable statistics relative to the frequency of cancer as a cause of death.’’ Cancer In ensuing decades, total cancer remained as a benchmark for accuracy of mortality studies, because of its importance and greater reliability, albeit not perfect, especially as different sites and varieties were compared. Barclay and Phillips in 1962 studied 7,146 deaths attributed to cancer in Saskatchewan and concluded that “Death Certificate diagnoses are insufficiently accurate to permit their use as a reliable indication of the incidence of cancer.” Lombard et al., in the same year, after study of 13,346 death records, came to a similar conclusion. In 1972, recalling Wells’ data 50 years earlier, Bauer and Robbins studied 10,977 autopsies at the Boston City Hospital. They found that only 60% of 2,734 reports confirmed a clinical diagnosis of cancer; 26.2% had undiagnosed cancer. Even in so carefully followed a group as Hiroshima and Nagasaki survivors, Steer and his colleagues [1973] estimated that in the 10,749 deaths occurring at home or in hospital, there were 32% more deaths due to cancer than certified on death certificate (3,095/2,345), a percentage not very different from that later found by Hasuo et al. [1989] in Hisayama, Japan, where 22% of the malignant neoplasms in 860 consecutive autopsies had an incorrect diagnosis on the death certificate. In a study with a different time-span, of 257 autopsy cases in a short-stay general hospital, Engel et al. [1980] found that malignant neoplasms were underreported approximately by 1096, with the death certificate inaccurate in 28%. An editorial in Human Pathology summarized the unease in 1987: “We are told that the mortality statistics generated by the NCI are the best we can do. There is no excuse for using unreliable data that lead to premature conclusions and obscure the truth. Even the most advanced computers, programmed by brilliant statisticians, cannot convert bad data into good data.” Autopsles as the Standard There have been suggestions that mortality rates could be derived from autopsy series despite the well-known selective bias inherent in such collections. To at least

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partially circumvent this constraint, Feinstein and Esdaile proposed [ 19871 that data should focus on unexpected conditions found at necropsy. As an example, “Necropsy discovery rate of coexisting but previously unsuspected lung cancer can be valuable.” Support for greater reliance on autopsy results in appreciating frequency of diseases has, at least in part, been based upon negative evidence of death certificate accuracy. A number of such reports have been detailed above. In addition, there have been repeated experiences in this regard, in many places and in a variety of facilities. Rigdon and Kirschoff [1963] reviewed 294 autopsied cases in a general hospital in Texas; 20% of the cancer cases and 32% of the general cases showed differences between the death certificate and post-mortem diagnoses. Britton [19741, studying 400 consecutive deaths in which 96% had autopsies, found that clinical diagnoses before death had been incorrect in 30%, and in 13% there were insufficient data to make a definitive diagnosis; clinical designation had been correct in only 57%. More recently, Cameron and McGoogan [ 198la,b] reviewed 1,152 autopsies (representing 25% of 5,633 hospital deaths) in hospitals in the South Lothian district of Scotland and found that certified clinical diagnoses agreed in only 61% of cases. These findings, moreover, were a “best case” estimate; the study was prospective, that is, a senior physician prepared dummy death certificates with access to clinical and pathological records. Neoplastic diseases were equally overdiagnosed and underdiagnosed (35%, 34%). As others, they were forced to conclude that “statistics from death certificates are so inaccurate that they are unsuitable for use in research or planning.” In Hawaii, too, among Japanese residents being followed, clinical impressions recorded on death certificates were frequently found inaccurate, only 61% being confirmed on autopsy [Stemmermann, 19821. The inaccuracies did not seem to vary over time, as might have been hoped with improved diagnostic technology. Study of 100 randomly selected autopsies for each of 1960, 1970, and 1980 at the Peter Bent Brigham Hospital in Boston showed that about one-quarter in each year had major discrepancies [Goldman et al., 19831. Unfortunately, too, as Kircher et al. have pointed out [ 19851, when autopsies provide a more accurate diagnosis, the information “is rarely used to supplement or revise the causes of death.” Hospital Records and Death Certificates

Perhaps comparing death certificate diagnoses with necropsy findings is too rigorous a test. It has therefore been considered worth reviewing a less stringent criterion-how well do death certificates reflect clinical observations available in hospital records? (Deaths out of hospital could not be as well expected to have fully adequate documentation.) Although this has been less frequently studied, results have not been encouraging. In 1981, Percy et al. reviewed the data of the Third National Cancer Survey, comparing hospital diagnoses with death certificates in 48,826 deaths. The death certificate was accurate in about 65% of the cancer deaths. Alderson and Meade [ 19671 found significant discrepancies between hospital records and death certificates in 39% of 1,216 hospital-based deaths, justifiable in only 7.2%. In Hawaii, Schwartz [1977] found gross errors on death certificates in 20% of 715 deaths, when compared with hospital discharge diagnoses. The percentages were even worse in 5 general hospitals in Kuwait [Moussa et al., 19901, and Cameron and McCoogan [ 1981a,b] did not find that diagnostic accuracy improved with time spent

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in hospital. In the Third National Cancer Survey, 1969-1971,73% of the deaths were in hospital, 12% in nursing homes, and 15% at home [Percy et al., 19811. It will be interesting to learn whether correlation of clinical findings with death certificatesvaries in the same way among deaths occurring in extended care facilities, in view of the increasing proportion of deaths occumng in such institutions in the past two decades, a trend likely to continue in the future.. Indeed, there is even concern that hospital records themselves may be declining in value. Burnum [1989] has written that such information “long flawed by errors introduced by medical personnel, patients, and machines” is being further distorted by being deliberately fashioned to keep sensitive personal information from public view. “For the gullible in medicine, this could well become the mis-information era,” despite the improvement in information machines.

An International Problem The foregoing comparisons have been made largely in Great Britain and the United States, two countries with well-developed, expertly staffed, knowledgeable, and experienced public health statistics agencies. Fewer reports are available from other lands or of the results of comparisons made among different countries. Findings in one of the best designed such studies were reported in 1978 [Percy and Dolman, 19781. There were 1,246 U.S. death certificates with cancer-relateddiagnoses sent to the Vital Statistics Departments of seven countries (Canada, France, Germany, Norway, United Kingdom, United States, the Soviet Union), using standard rules and codes (ICD-8). One or more of the participants gave a different underlying cause of death in 584/1,246 (47%). It was considered that perhaps the coding instructions were insufficiently clear, so new and more explicit rules were drafted; 25% still had one or more coding differences. Percy and Dolman studied coding questions. Lancet (leading article, 1966) has noted that such difficulties are amplified by international differences in terminology, diagnostic habits, and certifying practices. A number of countries have had significant, sometimes insurmountable, barriers to independent evaluations of correlations of death certificates and clinical and/or necropsy findings, with little or limited access to certificates suitable for correlative studies. In France, for example, Alies-Patin and Valleron [1985] “because of the anonymity of death certificates” had to investigate the mortality of workers at an asbestos-cement factory by using causes of death obtained from hospitals and family doctors. Even in Sweden, where the National Cancer Registry is frequently used for a variety of comparisons, in 1978, 1,634 death certificates (4.5%) with cancer as the underlying cause were unrecorded in the Registry. There was no information on how many cases of cancer appeared either on the death certificate or in the Cancer Registry [Mattsson and Wallgren, 19841. Twenty-five years ago, the U.S. National Center for Health Statistics [1967] ruefully noted that we did not have international agreement on procedures for classifying multiple causes of death and morbidity data or for indexing hospital records and that some doubt existed on the usefulness of attempts to compile statistics on causes of death because of difficulties of classification. As to the future, Major Greenwood was quoted: “The scientific purist who will wait for medical statistics until they are nosologically exact, is no wiser than Horace’s rustic waiting for the river to flow away.’’

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Notable Problems in Categorization In addition to international variations mentioned above, which, over time, can be minimized by diligent review and coordination, especially by such agencies as WHO and IARC, there are a number of categorizations which are almost generic to the question and which would have to be alertly sought out and accommodated. “Signal diseases.’’ Examples include previously rarely observed cancers which, within a short time, tend to become common as a result of some environmental change. Angiosarcoma associated with vinyl chloride exposure is one such; another is the recent zoonotic bovine spongiform encephalopathy (“Mad Cow Disease”) [Bradley, 19911and the human diseases of similar nature, kuru and Creutzfeld-Jacob disease [Gadjusek, 19911. A particularly pertinent example is mesothelioma. After its validation as a pathological entity by Klemperer and Rabin [1931], its rarity led a number of authoritative experts to still doubt its existence [Willis, 19601. It was not until Wagner et al. [1960] collected and reported 47 cases in South Africa that physicians and pathologists began to be alerted to the condition. It has been hoped that what transpired with mesothelioma could provide guidance on how long it takes to integrate new information of this sort into the corpus of knowledge needed for widespread diagnosis and certification. It is uncertain whether conclusions can yet be drawn. Newhouse and her colleagues have followed workers at an asbestos factory in London. In their first report [Newhouse and Wagner, 19691, pleural mesothelioma appeared on a death certificate in one of six such deaths (as established by review of available material) and peritoneal mesothelioma on three of 13. In 1985, Newhouse et al. reported that mesothelioma was misdiagnosed on death certificates in 40% of cases, despite this being a “best case” situation (known employment in an asbestos products factory, periodic prospective surveillance). In Glasgow , too, accuracy and completeness of mesothelioma recording were still being questioned in 1990. Of 113 cases identified by various agencies (hospitals, cancer registries, etc.), only 77 had appeared on death certificates [Gillis et al., 19901. This was an improvement, however, over the situation 20 years earlier. Then, there had been 70 cases microscopically verified in university and hospital pathology departments, 1950-1967. Only 9 of 22 cases categorized under this rubric 1955-1963 by the Registrar General for Scotland were included in the verified series [McEwen et al., 19701. Ducic of McGill [ 19713 reviewed 67 cases in Canada found to be mesothelioma on the basis of histological material. Death certificates were accurate in 10 (14.7%). More recently, in Detroit it was found [Nelson et al., 19871 that death certificates were accurate in 28.6% of malignant mesotheliomas, while nationally in the United States, only 23% of 776 pleural mesotheliomas and 20% of 146 peritoneal mesotheliomas were correctly recorded [Connelly et al., 19871.

The constraints posed by death certificate difficulties are well illustrated by recent Swiss experience. Minder and Vader [1988] utilized computer analysis of death certificates which mentioned “Code 163.0.” This resulted in an unexpected focus on “furniture workers” (excluding carpenters) and, therefore “a new high-risk group” was believed to have been identified. Schuler and Ruttner [1989] soon provided an alternate explanation. In their series of 160 cases of pleural mesothelioma,

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15 were in “furniture workers,” and asbestos was present in the lungs of 14, six having worked in railroad car construction and repair, with ample opportunity for asbestos exposure. Similar experienceswere detailed by Merler and Ricci [ 19891 with Italian railroad worker mesothelioma. Thus, designations as “furniture worker” and “upholsterers” included employees working on the asbestos-filled railroad carriages which had been built and insulated with asbestos. Generally, there is less diagnostic and, to that extent, classification difficulty with common diseases, particularly those that have been present for some time. This is not always true, however, either for the “older” occupational diseases or those which are widespread in the community. Silicosis, for example, has been recognized for over a century. Yet until 1930, the term was rarely used for certifying causes of death and even after that, the Home Office in the United Kingdom used the wider field of “fibrosis of the lung” “pulmonary disease due to dust,” as well as silicosis, to elucidate the incidence of the disease [Middleton, 19361. An even more troublesome example is the group of diseases often classified on death certificates as “chronic obstructive pulmonary disease.” The more one reads of the conditions which are often so labeled on certificates, the less sanguine one becomes that a resolution of the classification problem is in sight. It is now almost 40 years since Goodman et al. [1953] pointed out in Great Britain that “chronic bronchitis” covered a wide range of conditions from bronchiectasis or chronic bronchitis and emphysema to the degenerative conditions when used as a cause of death on death certificates. This was true in the United States and Canada as well, where diagnostic conventions played a role [Anderson, 19631. Perhaps because of such difficulties, there was much underreporting of the conditions; when certifiers of 3,193 U.S. deaths age 35-74 were queried for the presence and severity of chronic respiratory diseases, only half of these conditions were listed on the death certificates [Markush, 19681. Nomenclature also varied (and still does); Mitchell and his colleagues [ 19681 investigated deaths of “chronic airway obstruction” using autopsy data, and found both underreporting and overreporting. Terminology (and which entities to include) remains contentious. Coding, as might be expected, reflects the uncertainty. Thom [1989] pointed out that the 9th Revision of the International Classification included bronchitis, emphysema, and asthma but not the largest amount of COPD otherwise coded in the 8th Revision, and that “COPD mortality trends based on published WHO statistics between 1968 and the present are, therefore, not accurate for most countries and their level may be greatly understated.” Feinstein and his colleagues, in the same year [1989] also pointed to the serious impact that changes in reporting and classification had on comparability over time. Sometimes, such effects can be seen rather rapidly [Harvey et al., 19911. Other times, coding variations demonstrate their effects over decades [Marcus et al., 19891. Spiezer [1989], in a thoughtful overview, found that there was very poor concordance between clinical study diagnoses of COPD and death certificate diagnoses of the condition. “This calls into question the validity of COPD mortality statistics and suggests that COPD is considerably underdiagnosed on death certificates.” Further, classification is not made easier when occupation is added as another variable in the evaluation of chronic respiratory disease. Parenthetically, for those seeking a historical background to the uncertainties of classificationof this group of disease, it is instructive to read the personal experiences

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of Charles Fletcher [1978] during the deliberations of the Committee of Experts charged with developing appropriate terminology that would accurately describe and differentiate the various conditions. Age

There have been a number of reports which note that one factor which can influence accuracy of death certificate classification is age of the patients, with some older individuals less likely to have had fully adequate pre-mortem study despite greater likelihood of having complex clinical problems, often multiple and interacting. This may be important in occupational disease studies since disease outcomes are generally not discernible for considerable periods and mortality differences (compared to non-exposed comparison groups) not readily observed or statistically differentiated for 25 or more years from onset of exposure to the agents being investigated [Selikoff et al., 19801. This latency indicates that deaths from the diseases of interest will tend to occur among older workers; among asbestos insulation workers, for example, one-third of all deaths of lung cancer and mesothelioma and an even greater proportion of deaths of asbestosis have occurred after age 65 [Selikoff, 19901. To the extent, then, that advancing age might be associated with increasing inaccuracy of death certificates, additional uncertainties would be added to the use of death certificates for epidemiological study of occupational hazards. This may be especially true for these other studies, in which the possibility of selective bias might be increased [Selikoff and Seidman, 19911. Nevertheless, there is a paucity of observational data bearing on the question in general, still less in relation to occupational mortality investigations, and virtually none that would allow comparisons as to relative inaccuracies of death certificate diagnoses taking both disease categories and age into account. An analysis of the SEER Program database provided information on verification of different cancer diagnoses in different older ages. Histological material was more infrequent with advancing age, although the percentage examined at necropsy remained about the same [Muir, 19901. In several of the studies already quoted that showed discrepancies between death certificates diagnoses and autopsy findings, these increased with advancing age [Britton, 1974; Stemmermann, 1982; Hasuo et al., 19891. In contrast, two found the opposite. Goldman et al. [1983], at the Peter Bent Brigham Hospital in Boston, found missed clinical diagnoses “as high in adults below age 40 as in those above 65” and Cameron and McGoogan [ 1981bl found many of the discordant diagnoses in patients not of advanced age, occurring rather “over the wide range 40-93 years.” Rosenwaike and Logue found a high level of agreement (for whites) in a study of 3,000 deaths of individuals age 85 and over in New Jersey and Pennsylvania, except at age 100 and over. Structural Constraints A variety of explanations have been offered to account for the observed discrepancies between clinical and histopathological observations and recorded death certificate diagnoses. There was interest in this for many years [Kennaway and Kennaway, 19471. Some have been rather straight-forward, commonly experienced, but not easily avoided. To begin with, as Segarra [1979] points out, little training is provided in most medical schools on preparation of death certificates. Even if it were,

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doctors who enter information were educated at different medical schools over a period of more than 50 years and entries are certain to be of mixed terminology [NCHS, 19671. Terminology may be of importance as a result of other factors as well; for example, when McDonald and her colleagues [ 19831 studied the mortality experience of workers in an asbestos textile plant, they reported that 12 deaths were ascribed to “pneumoconioses” on death certificates and none to “asbestosis.” Confusion and differing opinions concerning the different categories of chronic lung disease have been discussed, as has the failure to collect and use all available records. This has recently been re-emphasized by Moriyama [ 19891. It is commonly recognized that there may be mechanical reasons why not all available data go into formulation of the death certificate. There may be a rush to complete the certificate [Carter, 19851 so as to allow burial arrangements to proceed, with clinical records sequestered in unidentified locations, or simply not be at hand, if death occurs at home. If pathological information is derived from necropsy study, it is supposed to be used to amend the death certificate. Often, it does not [Moriyama, 19891.

Other difficulties are somewhat less obvious, but nonetheless equally real and quantitatively perhaps more important. First, there is the basic question of lack of diagnostic criteria [Feinstein and Esdaile, 19871 and of a suitable standard by which quality can be measured [Moriyama, 19891, The fact that certificates received and processed by the National Center for Health Statistics are not reviewed [Carter, 19851 does not help matters. The NCHS is further bound to compile its statistics in compliance with World Health Organization regulations, using its International Cause of Death Classification system, sub-optimal for many bio-medical applications. The choice given to the certifying physician to designate “direct cause,” “underlying cause,” and “contributing conditions” is not always easy to make, especially when a majority of deaths occur in old age, with complicated combinations of diseases [Lindahl et al., 19901. Sometimes, the choice reflects judgement and a point of view [Moriyama, 19891 and can engender further uncertainty when the certifier has had little or no instruction on how to make such decisions in different circumstances. Another problem, not unrelated to the foregoing, is the convention that a single cause of death be recorded, even when there may be several diseases which might have acted individually or collectively to cause death [Feinstein and Esdaile, 19871. There have been no widely accepted approaches to remedy the situation. Even attempts at improvement of coding practices can introduce errors. An example may be given for lung cancer. Between 1963 and 1967, U.S.lung cancer deaths increased about 5.7% annually. In 1968, it nearly doubled, to 9.6%. In that year, there had been a change in coding rules and detailed review showed that an increase of 2.4% had simply been due to changes in classification or coding [Percy et al., 19741. Further, coding rules being followed is no guarantee that a “nosological number’’ will be translated into accurate prevalence data [Lilienfeld and Gunderson, 19861. Studies have been undertaken to see whether alternate or parallel diagnostic registers could amelioriate the death certificate problems or provide more accurate sets of data. The utility of the Social Security Systems 1% sample was found of limited applicability in epidemiological mortality studies [Goldsmith and Thresh, 19771. Some people had several social security numbers and, in other cases, deaths were not notified to the Social Security Administration. Moreover, only the fact of death was available with no breakdown by cause. Other administrative records have

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been considered, but they, too, were found inappropriate for the purpose [Aziz and Buckler, 19801. In Hawaii, two different coding sets were c o m p a r e d a e Honolulu Heart Program and that of the State Health Department. One showed a significant decline in deaths from Chronic Obstructive Pulmonary Disease and the other did not [Marcus et al., 19891. In South Africa, where deaths of mesothelioma are of much interest and tend to be well studied, 17 deaths of pleural mesothelioma were notified to the Department of National Health and Population from August 1979 to December 1983. This was 4% of the 458 such deaths registered at the central statistical services in the same period. Thus, the use of standard death registrations for pleural mesothelioma vastly underestimated its incidence [vanRensburg, 19871. ADVANTAGES IN USE OF DEATH CERTIFICATES

One might wonder, with this almost unrelieved litany of inadequate, uncertain, and variable accuracy of death certificates, why they continue to be used, even for occupational disease studies. One answer might be that death registrations based on completed certificates have a number of advantages which, unless and until a better process is introduced (and none has been so far and none are in the offing), should be utilized, even while improvements and modifications are undertaken. Thus, there is universal coverage, considerable uniformity, and standardization of processing. Coding errors are small (3-4% for medical items, in 1986) and rates are based upon large numbers of deaths, 2 million annually in the United States [CDC, 19891. This makes for stable age and sex specific death rates for total mortality. Hammond and Horn [1958] emphasized this in their studies on effects of cigarette smoking. “The most important finding of this study was the high degree of association between cigarette smoking and the total death rate. Errors in diagnosis, no matter how great, have no effect on this finding.” CONCLUSIONS

There has long been evidence of frequent inaccuracy of death certificates disease classifications, with significant disordance between such designations and clinical and autopsy data. This exists for occupational diseases as well. The use of statistical rates based upon death certificate notifications to provide the number of “expected” deaths for comparison with the number observed has been seriously questioned. Yet there are a number of advantages in the use of large scale (national, regional) death certificate data which should not be ignored, especiallly since satisfactory alternates to their use have not yet been forthcoming. Rather, programs to supplement death certificate data, particularly in occupational disease studies, may be useful [Selikoff and Seidman, 19911. REFERENCES Alderson MR, Meade TW (1967): Accuracy of diagnosis on death certificates compared with that in hospital records. Br J Prev Soc Med 21:22-29. Alies-Patin AM, Valleron AJ (1985): Mortality of workers in a French asbestos cement factory 1940-82. Br J Ind Med 42:219-225.

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Hasuo Y, Ueda K, Kiyohara Y, Wada J, Kawano H. Kato I, Yanai T, Fujii I, Omae T, Fujishima M (1989): Accuracy of diagnosis on death certificates for underlying causes of death in a long-term autopsy-based population study in Hisayama. Japan; with special reference to cardiovascular diseases. J Clin Epidemiol 42:577-584.

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