on causes of death, and these data are commonly ... the United States. .... generated from the original list of medical .... cancer as an associated cause of death.).
Causes of Death among Persons Reported with AIDS
Susan Y. Chu, PhD, James W. Buehler, MD, Loren Lieb, MPH, Geoff
Beckett, MPH, Lisa Conti, DVM, Sam Costa, MA, Beverley Dahan,
Richard Danila, PhD, MPH, E. James Fordyce, PhD, Ann Hirozawa, MPH, Anne Shields, RN, MHA, James A. Singleton, MS, and Cheryl Wold, MPH
Introduction
Methods
Vital statistics provide information on causes of death, and these data are commonly used to assess the impact of different illnesses and conditions on the health of populations. For example, in 1990 (the most current year such data are available), human immunodeficiency virus (HIV) infection was the second leading cause of death for young adult men (aged 25 to 44 years) and the sixth leading cause of death for young adult women in the United States.' This information has critically influenced the allocation of health resources for the prevention and treatment of HIV. Given the role of vital statistics in shaping national HIV policy, it is important to document their completeness in identifying HIV-related deaths. In 1989, the Centers for Disease Control and Prevention (CDC), in collaboration with state and local health departments, initiated a project to evaluate mortality in persons reported to have acquired iminunodeficiency syndrome (AIDS). A major component of this project involves linking information from death certificates with AIDS case records to examine causes of death among persons with AIDS. In this report, we describe the underlying and associated causes of death listed in the vital records of persons known to have AIDS, based on case reporting to state and local health departments. We examine trends in these causes over time, differences in listed causes by mode of HIV exposure, and the completeness with which HIV infection oi AIDS was reported on death cer-
Eleven health departments linked death certificates with local AIDS case reports to obtain cause-of-death information for persons reported with AIDS. Death certificates were obtained by local health departments from the vital registrar of the state in which the death occurred. To ensure complete ascertainment of deaths in persons reported with AIDS, each health department conducted a match of reported cases with the National Death Index for deaths occurring through December 1989. The National Death Index, which is operated by the National Center for Health Statistics (NCHS), is a
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Susan Y. Chu and James W. Buehler are with the National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Ga. Loren Lieb is with the Los Angeles County Department of Health Services, Calif. Geoff Beckett is with the Maine Department of Human Services, Augusta. Lisa Conti is with the Florida Department of Health and Rehabilitative Services, Tallahassee. Sam Costa is with the New Jersey Department of Health, Trenton. Beverley Dahan is with the Colorado Department of Health, Denver. Richard Danila is with the Minnesota Department of Health, Minneapolis. E. James Fordyce is with the New York City Department of Health, NY. Ann Hirozawa is with the San Francisco Department of Public Health, Calif. Anne Shields is with the Washington State Department of Health, Seattle. James A. Singleton is with the California Department of Health Services, Sacramento. Cheryl Wold is with the Boston Department of Health and Hospitals and the Massachusetts Department of Public Health. Requests for reprints should be sent to Susan Y. Chu, PhD, Division of HIV/AIDS, MSE-47, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA 30333. This paper was accepted March 23, 1993.
American Journal of Public Health 1429
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computerized index to death certificates on file in state vital statistics offices.2 The matching process identifies whether persons reported with AIDS have died and, through the index, provides the state and date of death and the corresponding death certificate number for each. In previous studies, the accuracy of the index match (i.e., the extent to which the mortality status of individuals has been correctly identified) has ranged between 80% and 990%34; accuracy is higher when social security numbers (available for five participating sites) are included in the matching criteria. The local health department can then obtain copies of death certificates from the appropriate state vital statistics
offices. Cause-of-death data are based on medical conditions recorded by physicians on death certificates and are coded by the NCHS and selected states using the International Classification of Diseases, 9th edition (ICD-9).5S6 These codes are then processed using a computer system that evaluates the list of medical conditions and selects the underlying cause of death based on rules contained in the ICD9.1 Associated causes of death are also generated from the original list of medical conditions. For 1983 through 1986, deaths attrbutable to HIV infection or AIDS were classified as ICD-9 code 279.1, "deficiency of cell-mediated immunity," the code implemented in 1983 for HIV/AIDS.6 In 1987, specific codes for HIV/AIDS (042 to 044) were introduced, alongwith new procedures for assigning HIV/AIDS as the underlying cause of death.7,8 Because of the change in classification of HIV-related deaths, cause-of-death data for 1987 and after are not directly comparable with data from 1983 through 1986.1 In particular, ICD-9 code 279.1 was not uniquely specific for HIV conditions, and other conditions were often selected instead as the underlying cause of death (e.g., Kaposi's sarcoma, Pnewnocystis carinu pneumonia). Consequently, we analyzed mortality data for 1983 to 1986 and for 1987 to 1989 separately. Other causes of death were grouped using the ICD-9. This analysis includes data collected through April 30, 1992, by 11 state/county health departments (California, Colorado, Florida, Los Angeles, Maine, Massachusetts, Minnesota, New Jersey, New York City, San Francisco, and Washington State) that obtained listed cause-of-death information on deaths occurring through 1989. Overall, these areas had complete cause-of-death information on 76% of 1430 American Journal of Public Health
their reported AIDS deaths (32 513/ 42 780); through the demographic data obtained from AIDS case reports it was determined that persons with and without complete cause-of-death data were similar by sex, race/ethnicity, age, and mode of HIV ex-posure. Deaths reported from these 11 areas represent 68% of all deaths among persons with AIDS reported in the United States during the same period (1983 to 1989).
Resuls For 12 949 persons with AIDS who died during 1983 to 1986 (before the specific codes for HIV/AIDS were introduced), 45.7% had "deficiency of cellmediated immunity" (ICD-9 279.1) listed as the underlying cause of death, and 36.5% of deaths were attributed to conditions within the 1987 AIDS surveillance definition. For 19 564 persons reported with AIDS who died during 1987 to 1989 (when new coding procedures for HIV were in effect),5 81.1% of death certificates listed HIV infection or AIDS (codes 042 to 044) as the underlying cause, and 80% of those listed codes 042.0 to 042.9, the subgroup that best approximates the 1987 AIDS surveillance definition. Because of the effects of the coding change, further analyses focus on mortality data collected after the new procedures were implemented-that is, during 1987 to 1989.
Reporting of HIV/AIDS on Death Certifiates (1987 to 1989 Deaths
Only) Of the 19 564 persons in our study, 17 290 (88%) had WHV/AIDS mentioned somewhere on their death certificates, including the 15 862 (81%) who had H1V infection or AIDS listed as the underlying cause of death (Table 1). Following HIV/ AIDS, the most common underlying causes ofdeath were individual conditions within the AIDS case definition (5%), among which Pnewnocystis cainri pneumoniawas the most frequent (41%). Other conditions listed as the underlying cause of death included pneumonia (excluding Pnewnocystis catinJi), infections not included in the AIDS surveillance case definition, other immune deficiencies, and drug abuse. Unintentional injuries, suicide, and homicide were less common (Table 1). Most cancers listed as the un-
derlying cause were AIDS-defining lymphomas or Kaposi's sarcoma (n = 68); others included lung cancer (n = 88),
Hodgkdn's disease (n = 19), and myeloid or lymphoid leukemia (n = 17). Reporting of HIV/AIDS on death certificates of persons with AIDS varied somewhat by race/ethnicity, sex, and HIV exposure category (Table 2). The sex and race differences primarily reflect differences in reporting by HIV exposure category. Reporting of HIV/AIDS on death certificates was the least complete among persons whose mode of exposure to HIV is unspecified. Reporting of HIV/AIDS on death certificates (any mention of HIV or AIDS) alsovaried by reporting area, ranging from 81% to 97%; differences by HIV exposure category were consistent within reporting areas.
Associated Causes ofDeath (1987 to 1989 Deaths Only) To examine associated causes of death, we reviewed multiple causes of death for the 15 862 persons for whom HIV/AIDS was listed as the underlying cause. In addition to listing HIV or AIDS, 42% of the certificates also listed a condition in the AIDS surveillance definition. The listing of these conditions varied by mode of exposure. For example, in addition to HIV or AIDS, a condition within the AIDS case surveillance definition was listed on 48% of death certificates of homosexual or bisexual men with AIDS; among injecting drug users and persons with AIDS attributed to heterosexual contact, the additional mention of an AIDSdefining condition was less frequent (31% and 28%, respectively). This partly reflects differences in the number of conditions reported on death certificates among persons in different HIV exposure groups; death certificates of homosexual and bisexual men with AIDS listed a median of three multiple causes, whereas death certificates of injecting drug users and persons with AIDS attributed to heterosexual contact listed a median of two causes. The most frequently listed causes outside the AIDS definition were ill-defined conditions (ICD-9 codes 780.0 to 799.9) (24%), pneumonia (13%), drug abuse (ICD-9 codes 292.0 to 292.9, 304.0 to 304.9, and 305.2 to 305.9) (12%), and sepsis (6%). Cervical cancer was listed in addition to HIV/AIDS on two death certificates; both deaths occurred among women reported to have had a blood transfusion. (Among 547 death certificates of women that did not list HIV/AIDS, 2 (0.4%) listed cervical cancer as an associated cause of death.) Certain associated causes were notably more frequent among certain HIV exposure groups. Of 1257 death certificates October 1993, Vol. 83, No. 10
Caue of AIDS Death
listing Kaposi's sarcoma, 96% were certificates of men with a histoxy of male-tomale sexual contact. Drug abuse was noted on 44% (1729/3910) of certificates among female and male heterosexual injecting drug users and on 10% of those among men reporting both injecting drug use and male-to-male sexual contact. In contrast, drug abuse was listed on less than 1% of certificates of men whose only riskwas male-to-male sexual contact, persons with hemophilia, and transfusion recipients. Hemophilia or other coagulation disorders were listed as an associated cause on 66% (49/74) of the certificates of adults and children who had coagulation disorders listed as the specified HIV exposure on the AIDS case report form; only one certificate listed hemophilia as an associated cause of death for which the exposure reported to AIDS surveillance was not coagulation disorder (a man reporting male-to-male sexual contact). October 1993, Vol. 83, No. 10
Causes of Death by Tine between Diagnosis and Death Causes of death also varied by time between diagnosis of AIDS and death. HIV/AIDS was more often listed as the underlying cause of death as the time between diagnosis and death increased (Table 3). This trend was consistent regardless of exposure category. The frequency of some associated conditions also vared by this criterion. Pnewnocystis carnu pneumonia was listed most often as a cause of death among persons who died in the same month they were diagnosed (including those who were diagnosed at death). The opposite trend was found for several other conditions. Kaposi's sarcoma, mycobacterial infections (including
Mycobacteinum aviwn), and cytomegalo-
virus disease were less frequent among those who died in the same month they were diagnosed and most frequent among those who died more than a year after diagnosis.
Discussion After specific HIV/AIDS codes were introduced in 1987, most (88%) death certificates of persons reported to national AIDS surveillance had HIV/AIDS listed as the underlying or an associated cause of death; in 81% of these deaths, HIV/AIDS was considered the underlying cause of death. Although cause-of-death information may not measure the full impact of American Journal of Public Health 1431
Chu et aL
disease in persons with AIDS, certain important patterns can be detected. For example, Pnewncysts cannu pneumonia was noted less often as a cause of death among persons who were diagnosed more than a year before death, which may reflect the effects of prophylaxis or treatment since it is often the initial AIDSdefining diagnosis and treatment is available. On the other hand, cytomegalovirus and mycobacterial infections were listed more often as a cause of death among persons diagnosed more than a year before death. These infections tend to occur later in the disease, and standard prophylaxis and therapeutic regimens were not available for them as for Pneumocystis carinu pneumonia.9 Previous analyses of HIV-related mortality have estimated that both AIDS surveillance and vital statistics identify 70% to 90% of HIV-related deaths in young adult men10 and 61% to 89% ofsuch deaths in young adult women.11 In January 1993, the CDC expanded the surveillance definition for AIDS in adults and adolescents, adding four new criteria in persons with documented HIV infection: a CD4+ T-lymphocyte count below 200/LL or percentage below 14, pulmonary tuberculosis, recurrent pneumonia, and invasive cervical cancer.12 Preliminary analyses have estimated that the 1993 AIDS surveillance definition will capture a higher percentage of HIV-related deaths (up to 98%), primarily from the addition of the CD4+ count criterion.13 However, neither system will identify deaths among persons in whom HIV infection or AIDS is not diagnosed, acknowledged, or reported, and therefore, they provide minimum estimates of mortality due to HIV infection.10,11,14,15 In this study, among persons reported with AIDS, the number of deaths due to major causes of death unrelated to HIV infection was relatively small, with less than 3% of deaths (based on underlying cause) due to drug abuse, injuries, suicide, homicide, and lung cancer. Although both AIDS surveillance and vital statistics have demonstrated dramatic increases in mortality due to HIV infection in the last decade, underestimates of the impact of HIV infection could diminish
1432 American Journal of Public Health
national, state, and local resources available for the prevention of HIV and the provision of health care and social services for HIV-infected individuals. Physicians and other health care professionals should be aware that the accuracy and completeness oftheir disease reporting ultimately can affect the distribution ofthese resources and the estimation of future public health needs for HIV-infected individuals.16-19 Ol
Acknowledgments This collaborative study also includes Joseph Bareta, MS (Maryland State Department of Health and Mental Hygiene), Denise Boyd, MPH (Arizona Department of Health), Todd Baumgartner, MD (Missouri Department of Health), Karen Edge, MPH (New Mexico Department of Health), and Barbara DeBuono, MD (Rhode Island Department of Health); their contributions are gratefilly acknowledged. The cooperation and assistance from several NCHS staff-in particular, Robert Bilgrad, Jerry Barber, Harry Rosenberg, PhD, Frances Chevarley, PhD, and Shirley Turbiville-were invaluable to the success of this project. We also thank Janet Kelly, MPH, Ruth Berkehnan, MD, and Meade Morgan, PhD, of the CDC; Tim Tyree and Teresa Jennings, MPA, in Washington; Tracy Spradling in Florida; Katy Young in San Francisco; Joan LeTourneau in Minnesota; Candace Wilson in Colorado; and Mi Chen in California for their valuable contributions.
References 1. Centers for Disease Control and Prevention. Update: mortality attnbutable to H1V infection/AIDS among persons 25-44 years, United States, 1990 and 1991.
MMWR 1993;42:481-485.
2. National Death Index User's ManuaL Hyattsville, Md: US Dept of Health and Human Services, National Center for Health Statistics; 1990. DHHS publication PHS 90-1148. 3. Patterson BH, Bilgrad R. Use of the National Death Index in cancer studies. JNatl Cancer Inst. 1986;77:877-881. 4. Williams BC, Demitrack LB, Fries BE. The accuracy of the National Death Index when personal identifiers other than social security number are used. Am J Public
Heakh 1992;82(8):1145-1147. 5. International Classification of Diseases, Manual of the International Statistical Classification of Diseases, Injuries, and Causes of Death. 9th revision. Geneva, Switzerland: World Health Organization; 1977.
6. National Center for Health Statistics. Vital Statistics ofthe United States, 1983. Vol 2. Mortalit, part A. Washington, DC: US Dept of Health and Human Services, Public Health Service; 1987. DHHS publication PHS 87-1101. 7. Centers for Disease Control. Human immunodeficiency virus (HIV) infection codes: official authorized addendum ICD9-CM (revision no. 1)-effective January 1, 1988. MMWR 1987;36(S-7):1-24. 8. Vital Statistics Data Preparation, National Center for Health Statistics. Instruction Manual Part 2a. Insnsctions for Classifying the Underlyi Cause of Death, 1989. Hyattsville, Md: National Center for Health Statistics; 1989. 9. Horsburgh CR. Mycobacterinum avium complex infection in the acquired immunodeficiency syndrome. NEnglJMed. 1991;
324:1332-1338. 10. Buehler JW, Devine OJ, Berkelman RL, Chevarley FM. Impact of the human immunodeficiency virus epidemic on mortality trends inyoung men, United States. Am JPublic Health. 1990;80:1080-1086. 11. Buehler JW, Hanson DL, Chu SY. The reporting of HIV/AIDS deaths in women. Am J Public Health. 1992;82(11):15001505. 12. Centers for Disease Control and Prevention. 1993 revised classification system for HIV infection and expanded surveillance case definition for AIDS among adolescents and adults. MMWR 1992;41(RR-
17):1-19. 13. Chu SY, Hanson DL, Fanzo KM, Buehler JW, Ward JW. Capturing HIV-related mortality: effect of the 1993 expanded AIDS surveillance definition. Presented at the Ninth International Conference on AIDS; June 6-11, 1993; Berlin, Germany. Abstract No. WS-C01-5. 14. Hessol NA, Buchbinder SP, Colbert D, et al. Impact of HIV infection on mortality and accuracy of AIDS reporting on death certificates. Am J Public Health. 1992;
82(4):561-564. 15. Chu SY, Buehler JW, Berkelman RL. Impact of the human nimunodeficiencyvirus epidemic on mortality in women of reproductive age, United States. JAMA. 1990; 264:225-229. 16. Goodman RA, Berkelman RL. Physicians, vital statistics, and disease reporting.
JAMA 1987;258:379-380. 17. Rosenberg HM. Improving cause-of-death statistics. Am JPublic Heakh. 1989;79(4): 563-564. 18. McCormick A. Trends in mortality statistics in England and Wales with particular reference to AIDS from 1984 to April 1987. Br Med J. 1988;296:1289-1292. 19. Kelly JJ, Chu SY, Buehler JW, and the AIDS Mortality Project Group. AIDS deaths shift from hospital to home. Am J Public Health. 1992;83:1433-1437.
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