Background With China's rapid economic development, the diseaseburden may have changed in the country. We studied the majorcauses of death and modifiable risk factors in a nationallyrepresentative cohort of 169,871 men and women 40 years of ageand older in China.
Methods Baseline data on the participants' demographic characteristics,medical history, lifestyle-related risk factors, blood pressure,and body weight were obtained in 1991 with the use of a standardprotocol. The follow-up evaluation was conducted in 1999 and2000, with a follow-up rate of 93.4 percent.
Results We documented 20,033 deaths in 1,239,191 person-yearsof follow-up. The mortality from all causes was 1480.1 per 100,000person-years among men and 1190.2 per 100,000 person-years amongwomen. The five leading causes of death were malignant neoplasms(mortality, 374.1 per 100,000 person-years), diseases of theheart (319.1), cerebrovascular disease (310.5), accidents (54.0),and infectious diseases (50.5) among men and diseases of theheart (268.5), cerebrovascular disease (242.3), malignant neoplasms(214.1), pneumonia and influenza (45.9), and infectious diseases(35.3) among women. The multivariate-adjusted relative riskof death and the population attributable risk for preventablerisk factors were as follows: hypertension, 1.48 (95 percentconfidence interval, 1.44 to 1.53) and 11.7 percent, respectively;cigarette smoking, 1.23 (95 percent confidence interval, 1.18to 1.27) and 7.9 percent; physical inactivity, 1.20 (95 percentconfidence interval, 1.16 to 1.24) and 6.8 percent; and underweight(body-mass index [the weight in kilograms divided by the squareof the height in meters] below 18.5), 1.47 (95 percent confidenceinterval, 1.42 to 1.53) and 5.2 percent.
Conclusions Vascular disease and cancer have become the leadingcauses of death among Chinese adults. Our findings suggest thatcontrol of hypertension, smoking cessation, increased physicalactivity, and improved nutrition should be important strategiesfor reducing the burden of premature death among adults in China.
Rapid economic development and the consequent improvement inliving conditions, nutrition, and health care have resultedin declines in infant mortality and deaths from infectious diseasesand therefore in increases in life expectancy in many developingcountries, including China.1,2 In contrast, adverse changesin lifestyle (such as a high intake of dietary fat and increasedphysical inactivity) that tend to accompany industrializationand urbanization have become increasingly prevalent in thesecountries, and such changes may have increased the risk of chronicdisease, including vascular disease and cancer.2,3,4 However,there are few data to support this epidemiologic transitionof disease burden in developing countries.1 Unlike the situationin developed countries, in developing countries valid data onvital statistics are not usually available, owing to a lackof coherent systems for national registration of deaths.5
Cross-sectional studies, which provide a point estimate of diseaseburden, have indicated that the prevalence of chronic diseasesand their risk factors has increased in developing countries.6,7,8However, large, prospective cohort studies involving representativesamples of the general population are needed to provide validinformation on cause-specific mortality in the populations ofthese countries and to provide a scientific basis for rationalallocation of health care resources. We conducted a large, prospectivecohort study involving a representative sample of the generaladult population 40 years of age and older in China to determinecause-specific mortality and to examine major preventable riskfactors for total mortality.
Methods
Study Population
In 1991, a multistage, random cluster-sampling design was usedto identify a representative sample of the general Chinese population15 years of age and older from all 30 provinces for the ChinaNational Hypertension Survey.9 In 1999, investigators from eachprovince were invited to participate in the China National HypertensionSurvey Epidemiology Follow-up Study. Of the 30 provinces includedin the initial study, 13 were not included in the follow-upstudy because contact information for the study participantsin those provinces was not available. However, sampling wasconducted independently within each province for the 1991 ChinaNational Hypertension Survey, and study participants in the17 provinces that were included in the follow-up study wereevenly distributed among the different geographic regions ofthe entire country representing various stages of economic development.Therefore, our study participants probably represent the generaladult population in China. Overall, 83,533 men and 86,338 womenwho were 40 years of age or older at the time of their baselineexaminations were eligible for participation in the follow-upstudy. Of these, a total of 158,666 participants or their proxies(93.4 percent) were identified and interviewed as part of thefollow-up study.
Baseline Examination
Baseline data were collected during a single clinic visit byphysicians and nurses trained in the use of standard methodsand with stringent quality control.9 Data on demographic characteristics,medical history, and lifestyle-related risk factors were obtained.The assessment of physical activity involved only work-relatedphysical activity. Cigarette smoking was defined as smokingat least one cigarette per day for one or more years. Data werecollected on the amount and type of alcohol consumed duringthe previous year.
Three blood-pressure readings, measured with the use of a mercurysphygmomanometer according to a standard protocol, were obtainedafter the participant had been sitting quietly for five minutes.10The first and fifth Korotkoff sounds were recorded as systolicand diastolic blood pressure, respectively. Hypertension wasdefined as one or more of the following: a mean systolic bloodpressure greater than or equal to 140 mm Hg, a mean diastolicblood pressure greater than or equal to 90 mm Hg, or the useof antihypertensive medication.11 Body weight and height weremeasured when the participant was wearing light indoor clothingbut not shoes, with the use of a standard protocol. Underweightwas defined as a body-mass index (the weight in kilograms dividedby the square of the height in meters) of less than 18.5 andoverweight or obesity as a body-mass index of 25.0 or greater.12
Follow-up Data
Follow-up examinations, which were conducted in 1999 and 2000,included tracking participants or their proxies to a currentaddress; conducting in-depth interviews to obtain informationon the history of disease, hospitalizations, and death; andobtaining hospital records and death certificates. All deathsidentified in interviews with participants' proxies were verifiedby death certificates obtained from the local departments ofpublic health or police. If death occurred while a participantwas hospitalized, the participant's hospital records, includingmedical history, findings on physical examination, laboratoryfindings, autopsy findings, and discharge diagnosis, were abstractedby trained staff using a standard form. In addition, photocopiesof selected sections of the participant's inpatient record,discharge summary, electrocardiogram, and pathology reportswere obtained.
An end-point assessment committee in each province reviewedand confirmed (or rejected) the hospital's discharge diagnosisand the cause of death on the basis of the abstracted information,using prespecified criteria. A study-wide end-point assessmentcommittee at the Chinese Academy of Medical Sciences in Beijingreviewed all death records and determined the final underlyingcause of death. Two committee members independently of eachother verified the cause of death, and discrepancies were adjudicatedby discussion involving other members of the committee. Allmembers of the local and study-wide end-point assessment committeeswere unaware of information about the baseline risk factorsof the study participants. The causes of death were coded accordingto the International Classification of Diseases, Ninth Revision(ICD-9).
The current study was approved by the Tulane University HealthSciences Center's institutional review board. Written informedconsent was obtained from all study participants at their follow-upvisit.
Statistical Analysis
Person-years of follow-up were calculated for each study participantand grouped according to sex and to age in five-year categories.Age-standardized mortality was calculated with the use of thefive-year age-specific mortality and the age distribution ofthe Chinese population, obtained from the 2000 census data.Age-standardized cause-specific mortality was calculated separatelyfor men and women, for residents of urban and rural areas, andfor those living in northern and southern China, where dietand other lifestyle-related risk factors were different.13 Forexample, the dietary intake of sodium was higher among residentsof northern China, as compared with those of southern China,whereas physical activity was lower.
Cox proportional-hazards models were used to estimate the relativerisk of death for preventable risk factors. Heavy alcohol consumption(i.e., three or more drinks per day) was not related to an increasein total mortality, but we included alcohol consumption as acovariate because it was strongly related to other risk factorsincluded in the study. A self-reported history of diabetes wasalso included as a covariate, because it was significantly associatedwith total mortality. Because the total mortality for currentand former cigarette smokers was similar, the relative riskof ever having smoked as compared with never having smoked wascalculated. As compared with normal weight (a body-mass indexof 18.5 to 24.9), overweight or obesity was not associated withincreased mortality. In contrast, because underweight was associatedwith increased total mortality, the relative risk of underweightwas estimated.
In the final multivariate models, all preventable risk factors,such as hypertension, cigarette smoking, physical inactivity,and underweight, as well as the covariates, including baselineage, sex, the presence or absence of a high-school education,alcohol consumption, self-reported history of diabetes, geographicregion (north vs. south), and urbanization (urban vs. ruralresidence), were included simultaneously. The population attributablerisk, measured as the percentage of deaths that could be preventedin the total population if the risk factor of interest wereeliminated, was calculated.14 Statistical analyses were conductedwith the use of SAS software, version 8 (SAS Institute).
Results
The baseline characteristics of the study participants accordingto sex are presented in Table 1. Overall, 49.2 percent of thestudy participants were men and 50.8 percent were women. Themean age was 55.8 years, with a range from 40 to 105 years.
Table 1. Baseline Characteristics of the 169,871 Study Participants.
During an average follow-up period of 8.3 years (1,239,191 person-years),we documented 20,033 deaths. The total mortality was 1345.2per 100,000 person-years (1480.1 per 100,000 person-years amongmen and 1190.2 per 100,000 person-years among women). Age-standardizedmortality and the percentage of total deaths for the 10 leadingcauses of death are shown in Table 2. The three leading causesof death (diseases of the heart, malignant neoplasms, and cerebrovasculardisease) accounted for 66.0 percent of deaths from all causes(68.7 percent in men and 62.6 percent in women).
Table 2. Age-Standardized Mortality and the Percentage of Total Deaths for the 10 Leading Causes of Death in China.
The five leading causes of death from vascular disease werecerebrovascular disease (mortality, 276.9 per 100,000 person-years),chronic pulmonary heart disease (137.6), coronary heart disease(85.5), heart failure (14.5), and rheumatic heart disease (9.7).(The International Classification of Diseases, 9th Revision,code for chronic pulmonary heart disease is 416, and the codesfor rheumatic heart disease are 391 through 398.) The rank orderof deaths from vascular disease was consistent in men and women(Figure 1). The five leading causes of death from cancer weremalignant neoplasms of the lung (mortality, 71.5 per 100,000person-years), liver (54.7), stomach (48.6), esophagus (31.3),and colon and rectum (17.4). However, stomach cancer was thesecond leading cause of death from cancer among women (Figure 1).Among women, mortality from malignant neoplasm of the breastwas 11.1 per 100,000 person-years and from malignant neoplasmof the uterus was 18.0 per 100,000 person-years.
Figure 1. Age-Standardized Mortality for the Five Leading Causes of Death from Vascular Disease (Panel A) and Malignant Neoplasms (Panel B) among 169,871 Study Participants.
Chronic pulmonary heart disease (cor pulmonale) is an abnormality of right ventricular structure or function, which in China is usually caused by chronic obstructive pulmonary disease.
Age-specific mortality for the five leading causes of death(40 to 64 years of age vs. 65 years of age or more) and age-standardizedmortality according to urbanization (urban vs. rural) and geographicregion (north vs. south) are shown in Figure 2. The patternof cause-specific mortality was consistent between men and women(data not shown). Overall, diseases of the heart, malignantneoplasms, and cerebrovascular disease accounted for more thanhalf of deaths from all causes in each subgroup. For example,the percentages of total deaths due to these causes were 62.1percent among older study participants and 71.4 percent amongyounger participants, 70.3 percent among urban residents and61.7 percent among rural residents, and 75.2 percent among thoseliving in northern China and 53.9 percent among those livingin southern China. Deaths from diseases of the heart and cerebrovasculardisease were significantly higher in northern China than insouthern China.
Figure 2. Age-Specific or Age-Standardized Mortality for the Five Leading Causes of Death among Study Participants 65 Years of Age or Older or Younger Than 65 Years (Panel A), Those Who Were Urban or Rural Residents (Panel B), and Those Living in Northern or Southern China (Panel C).
Diseases of the heart classified according to the International Classification of Diseases, Ninth Revision (ICD-9) include acute rheumatic fever (ICD-9 codes 390 through 392), chronic rheumatic heart disease (ICD-9 codes 393 through 398), hypertensive disease (ICD-9 codes 401 through 405), ischemic heart disease (ICD-9 codes 410 through 414), diseases of the pulmonary circulation (ICD-9 codes 415 through 417), and other forms of heart disease (ICD-9 codes 420 through 429). Age-specific mortality is shown in Panel A, and age-standardized mortality in Panels B and C.
The multivariate adjusted relative risk and population attributablerisk of death for major preventable risk factors are presentedin Table 3. Hypertension appeared to be responsible for 11.7percent of the total mortality in the study population. Thisestimated population attributable risk did not vary substantiallyaccording to sex, urbanization, or geographic region. Cigarettesmoking was responsible for 7.9 percent of the total mortality;the estimated risk was higher among men than among women andhigher among urban residents than among rural residents. Physicalinactivity accounted for 6.8 percent of the total mortality,with the estimated risk of death being slightly higher amongmen than among women and higher among urban residents than amongrural residents (especially among women). Underweight accountedfor 5.2 percent of the total mortality; the estimated risk ofdeath was consistent between men and women, but it was higheramong rural residents than among urban residents, and higheramong those living in southern China than among those in northernChina. The association between underweight and an increasedrisk of death remained significant after the exclusion of studyparticipants who were current or former smokers; those who hadprevalent cardiovascular disease, stroke, cancer, or end-stagerenal disease; those who had chronic obstructive pulmonary diseaseat the baseline examination; or those who died during the firstthree years of follow-up.
Table 3. Relative Risk and Population Attributable Risk of Death Associated with Hypertension, Cigarette Smoking, Physical Inactivity, and Underweight in China.
Discussion
Our study indicates that diseases of the heart, malignant neoplasms,and cerebrovascular disease are the leading causes of deathin the Chinese population of adults 40 years of age and older.Together, these causes accounted for approximately two thirdsof the total mortality in the study population.
These findings have important public health implications. Historically,infant mortality and death from infectious diseases have beenthe major causes of death in developing countries.15 Even inrecent years, the public health priorities, which are set bygovernment policymakers in these countries and by internationalagencies, have been to reduce infant and maternal mortalityand to control infectious diseases.16,17 The results of thepresent study call for serious attention to be given to theconsequences of chronic diseases in developing countries.
Few previous studies have reported cause-specific mortalityin China.18,19,20 According to vital statistics available for13 cities in China, diseases of the respiratory system, acuteinfectious diseases, and tuberculosis were the leading causesof death in 1957, accounting for 16.9 percent, 7.9 percent,and 7.5 percent of the total deaths, respectively. In the sameperiod, diseases of the heart, cerebrovascular disease, andmalignant neoplasms were the fifth, sixth, and seventh leadingcauses of death, accounting for 6.6 percent, 5.5 percent, and5.2 percent of total deaths, respectively.18 Although thereare differences in the reporting and classification of deathsbetween these studies and ours, our data support the notionthat a transition in disease burden has occurred in China.
Typically, chronic diseases have been considered a public healthproblem only in developed countries and among the elderly.3Our study suggests that chronic diseases affect a much higherproportion of people during their prime working years in China,as compared with developed countries.21 For example, the mortalitywas 265.9 per 100,000 person-years for malignant neoplasm, 171.5per 100,000 person-years for cerebrovascular disease, and 159.1per 100,000 person-years for diseases of the heart in the Chinesepopulation 40 to 64 years of age in our study. In the U.S. population45 to 64 years of age, the corresponding mortality rates in2002 were 215.1, 23.8, and 150.5 per 100,000 person-years.21The economic impact of chronic disease on society, includingthe direct costs of health care and the indirect costs resultingfrom lost productivity due to illness and death, is substantial.The higher number of deaths due to chronic disease among ruralresidents, as compared with urban residents, in China is a particularconcern because of the scarce health care resources availablein rural China and the fact that infant mortality and infectiousdiseases remain serious public health challenges in this setting.
Hypertension is the most common risk factor for cardiovascularand cerebrovascular diseases worldwide.6 The prevalence of hypertensionhas been increasing in China in recent decades, whereas ratesof awareness, treatment, and control remain unacceptably low.22Our results indicate that hypertension is the leading preventablerisk factor for death among Chinese adults 40 years of age andolder; total mortality was 48 percent higher among study participantswho had hypertension than among those who did not have hypertension.Furthermore, our findings suggest that the prevention and controlof hypertension could reduce the total mortality by 11.7 percentin the total study population. These results are consistentwith other analyses that have suggested that hypertension isthe leading risk factor for the global burden of disease.3,4
Our study also indicates that cigarette smoking is a major preventablerisk factor for death in China. If cigarette smoking were eliminated,we estimate that the total mortality could be reduced by 10.0percent among men and by 3.5 percent among women in China. Thisestimate does not take into account the possible effects ofpassive smoking.23 Our data are in agreement with those fromseveral prospective cohort studies and case controlstudies conducted in China, which have documented that cigarettesmoking increases the mortality from cancer, respiratory disease,and cardiovascular disease.24,25,26,27,28 Although our studydid not detect a significant difference in total mortality betweencurrent and former smokers, epidemiologic investigations indicatethat a reduction in mortality occurs gradually after smokingis stopped.29 In our study, the average interval since a participanthad stopped smoking was only seven years. In addition, we foundthat physical inactivity was related to an increase in totalmortality in China. These findings suggest that increasing physicalactivity could play an important role in the reduction of totalmortality in China.
Finally, our study identified underweight as a preventable riskfactor for total mortality. The population attributable riskfor underweight was slightly higher among rural residents thanamong urban residents. Underweight, which may reflect malnutrition,was reported as the leading cause of the disease burden in developingcountries with high mortality and an important contributor tothe burden of disease in developing countries with low mortality,in a recent report from the World Health Organization.30
Some limitations of our study should be noted. We did not collectdata on dietary patterns, leisure-time physical activity, serumlipid levels or results of other laboratory tests, or changesin body weight (or changes in other risk factors) over time.Therefore, the contribution of these factors to total mortalitycould not be estimated. A diagnosis of diabetes was based onlyon self-reports; it is likely that this resulted in an underestimationof the population attributable risk of death due to diabetes.The lack of autopsy data to confirm causes of death may haveintroduced some misclassification bias. However, we maintaineda very high follow-up rate and used a stringent approach toclassifying outcomes on the basis of medical records.
In summary, our study indicates that diseases of the heart,malignant neoplasms, and cerebrovascular disease account forapproximately two thirds of the total deaths in the Chinesepopulation 40 years of age and older. Furthermore, hypertension,cigarette smoking, physical inactivity, and underweight areleading preventable risk factors for death. Control of hypertension,smoking cessation, increased physical activity, and improvednutrition are likely to be important strategies for reducingthe burden of mortality in China.
Supported by grants from the American Heart Association (9750612N),the National Heart, Lung, and Blood Institute (U01 HL072507),and the Chinese Academy of Medical Sciences (Beijing).
All investigators participating in this study are listed inthe Appendix.
* Drs. He and Gu contributed equally to this work.
Source Information
From the Department of Epidemiology, Tulane University School of Public Health and Tropical Medicine (J.H., K.R., C.-S.C., J.C., R.P.W., P.K.W.), and the Department of Medicine, Tulane University School of Medicine (J.H., J.C., P.K.W.) both in New Orleans; the Cardiovascular Institute, Fuwai Hospital of the Chinese Academy of Medical Sciences and Peking Union Medical College, and the National Center for Cardiovascular Disease Control and Research, Beijing (D.G., X.W., X.D.); Anzhen Hospital, Capital University of Medical Sciences, Beijing (C.Y.); West China College of Medicine, Sichuan University, Chendu, China (J.W.); and the Department of Medicine, Johns Hopkins University School of Medicine, Baltimore (M.J.K.).
Address reprint requests to Dr. He at the Department of Epidemiology, Tulane University School of Public Health and Tropical Medicine, 1430 Tulane Ave., Mail Stop SL18, New Orleans, LA 70112, or at jhe{at}tulane.edu.
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Appendix
The following investigators participated in this study: SteeringCommittee: J. He (coprincipal investigator), D. Gu (coprincipalinvestigator), J. Chen, R. Hui, M.J. Klag, L. Kong, S. Tao,J. Wang, P.K. Whelton, X. Wu, and C. Yao; Participating Institutionsand Principal Staff: Tulane University Health Sciences Center,New Orleans: C.-S. Chen, J. Chen, J. He, K. Reynolds, P.K. Whelton,R.P. Wildman; Johns Hopkins Bloomberg School of Public Health,Baltimore: M.J. Klag; Fuwai Hospital and Cardiovascular Institute,Chinese Academy of Medical Sciences, and Peking Union MedicalCollege, Beijing: X. Duan, W. Gan, D. Gu, G. Huang, S. Tao,X. Wu, W. Yang, J. Zhao; Chinese Ministry of Health, Beijing:L. Kong; Tianjin City Bureau of Public Health, Tianjin, China:G. Zheng; Tianjin City Center of Disease Control and Prevention,Tianjin, China: G. Song; Guangdong Provincial People's Hospitaland Cardiovascular Institute, Guangdong, China: X. Liu, J. Mai;Anzhen Hospital, Capital University of Medical Sciences, andBeijing Institute of Heart, Lung, and Blood Vessel Diseases,Beijing: C. Yao; Capital Iron and Steel Company's Hospital,Beijing: X. Yu; Fangshan District Hospital, Beijing: X. Xu;Zhejiang Provincial Center for Cardiovascular Disease Preventionand Research, Zhejiang, China: H. Jin, X. Tang; Fujian ProvincialPeople's Hospital, Fujian, China: X. Pu, L. Yu; Shandong ProvincialAcademy of Medical Sciences, Shandong, China: S. Zhang; GuangxiMedical University, Guangxi, China: L. Zhu; Xi'an Jiaotong UniversityMedical School, Shanxi, China: J. Mo; Henan Provincial Academyof Medical Sciences, Henan, China: J. Guo; Tongji Medical Collegeand School of Public Health, Huazhong University of Scienceand Technology, Hubei, China: Y. Hu, Y. Yu; Sichuan ProvincialCenter of Disease Control and Prevention, Sichuan, China: X.Wu; West China College of Medicine, Sichuan University, Sichuan,China: J. Wang; Nanjing Medical University, Jiangsu, China:H. Shen, C. Yao; Beihua University Medical School, Jilin, China:L. Xu, G. Zhao; Inner Mongolia Hospital, Inner Mongolia, China:X. Gao, J. Zhou; First Clinical College of Harbin Medical University,Heilongjiang, China: Y. Li; Daqing City Center of Disease Controland Prevention, Heilongjiang, China: Z. Li; Hebei ProvincialAcademy of Medical Sciences, Hebei, China: H. Zhang; ZhongshanHospital and Institute of Cardiovascular Diseases, Fudan University,Shanghai, China: X. Pan.
Major Causes of Death in China
Wagner P. D., Viegi G., Luna C. M., Fukuchi Y., Kvale P. A., Sony A. E., Wei M., Wang K., Wang B., Barnett V. T., He J., Gu D., Whelton P. K.
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