A Population-Based, Prospective Study of Blood Pressure and Risk for End-Stage Renal Disease in China
Kristi Reynolds*,
Dongfeng Gu,
Paul Muntner*,,
John W. Kusek,
Jing Chen,
Xigui Wu,
Xiufang Duan,
Chung-Shiuan Chen*,
Michael J. Klag||,
Paul K. Whelton*, and
Jiang He*,
* Department of Epidemiology, School of Public Health and Tropical Medicine; Department of Medicine, School of Medicine, Tulane University, New Orleans, Louisiana; Cardiovascular Institute and Fuwai Hospital of the Chinese Academy of Medical Sciences and Peking Union Medical College, and Chinese National Center for Cardiovascular Disease Control and Research, Beijing, China; National Institute of Diabetes and Digestive and Kidney Diseases, Bethesda, Maryland; and || Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland
Address correspondence to: Dr. Kristi Reynolds, Department of Epidemiology, Tulane University School of Public Health and Tropical Medicine, 1440 Canal Street, Suite 2036, New Orleans, LA 70112. Phone: 504-988-6972; Fax: 504-988-7448; kristi.reynolds{at}tulane.edu
Received for publication November 3, 2006.
Accepted for publication March 19, 2007.
The association between BP and risk for ESRD has not been wellcharacterized in Asian populations. This study examined therelationship between level of BP and incidence of ESRD in aprospective cohort study of 158,365 Chinese men and women whowere 40 yr and older. Measurement of BP and covariables weremade in 1991 following a standard protocol. Follow-up evaluationswere conducted in 1999 to 2000 and included interviewing participantsor proxies and obtaining medical records and death certificatesfor ESRD cases. During 1,236,422 person-years of follow-up,380 participants initiated renal replacement therapy or diedfrom renal failure (30.7 cases per 100,000 person-years). Comparedwith those with normal BP, the multivariate adjusted hazardratios (95% confidence interval) of all-cause ESRD for prehypertensionand stage 1 and stage 2 hypertension were 1.30 (0.98 to 1.74),1.47 (1.06 to 2.06), and 2.60 (1.89 to 3.57), respectively (P< 0.001 for trend). The corresponding hazard ratios (95%confidence interval) of glomerulonephritis-related ESRD were1.32 (0.82 to 2.11), 1.48 (0.83 to 2.61), and 3.40 (2.02 to5.74), respectively (P <0.001 for trend). Systolic BP wasa stronger predictor of ESRD than diastolic BP or pulse pressure.This study provides novel data on the incidence of ESRD andon the association between BP and glomerulonephritis-relatedESRD from a nationally representative sample of adults in China.These results document the importance of high BP as a modifiablerisk factor for ESRD in China. Strategies to prevent ESRD shouldincorporate the prevention, treatment, and control of BP.
The number of patients who have ESRD and are treated by renalreplacement therapy, dialysis, or transplantation has been increasingin the United States and worldwide (1,2). The number of incidentand prevalent ESRD cases in the United States is projected torise from 93,000 and 382,000, respectively, in 2000 to 136,166and 712,290, respectively, by 2015 (3). The burden of ESRD inChina and other economically developing countries is less wellknown.
Although hypertension is widely recognized as an independentrisk factor for the development and progression of chronic kidneydisease (4,5), few prospective studies have examined the riskfor ESRD across a broad range of BP levels (6–9). Furthermore,the relationship between elevated BP and the development ofESRD has not been characterized in China, where national surveysof hypertension have indicated that the prevalence of hypertensionis high and increasing (10,11). Data from the InternationalCollaborative Study of Cardiovascular Disease in Asia indicatethat 27.2% of adults (129.8 million adults) aged 35 to 74 yrin China had hypertension in 2000 to 2001 (11). At the sametime, the prevalence of awareness, treatment, and control ofhypertension was only 44.7, 28.2, and 8.1%, respectively (11).
In China, glomerulonephritis is the most common underlying assignedcause for ESRD, whereas in the United States, it accounts foronly 8% of new cases (2,12). A better understanding of modifiablerisk factors for ESRD in China is important for targeting limitedhealth care resources and for the development and implementationof national prevention strategies. We conducted a prospectivecohort study in China to determine the incidence and relativerisk for ESRD across a wide range of BP levels; to compare therelative importance of systolic BP (SBP), diastolic BP (DBP),and pulse pressure on the incidence of ESRD; and to examinewhether the risk that is imposed by BP is consistent for glomerulonephritis-and non–glomerulonephritis-related ESRD.
Study Population
In 1991, a multistage, random-cluster sampling design was usedto select a representative sample of the general Chinese populationfor the China National Hypertension Survey (10). A total of950,356 men and women who were 15 yr and older were selectedfrom all 30 provinces. In 1999, 17 of the 30 provinces participatedin the China National Hypertension Survey Epidemiology Follow-upStudy (CHEFS). Thirteen provinces were not included in the follow-upstudy because participants’ contact information was notavailable. However, sampling for the 1991 survey was conductedindependently within each province, and participants who wereincluded in the follow-up study were evenly distributed amongthe different geographic regions of the entire country, representingvarious stages of economic development. Overall, 169,871 participants(83,533 men and 86,338 women) who were 40 yr or older at thebaseline examination were eligible for the follow-up study.From this population, a total of 158,666 (93.4%) participantsor their proxies were identified and interviewed as part ofthe follow-up study. After exclusion of those with ESRD at baseline(n = 34) and those with missing BP measures (n = 267), datafrom 158,365 participants were included in this analysis.
Baseline Examination
Baseline data collection occurred during a single visit to alocal field center. Information on demographic characteristics,medical history, and lifestyle risk factors were obtained usinga standard questionnaire that was administered by trained staff.Physical activity was assessed using a questionnaire that askedparticipants about their work-related activities. Leisure-timephysical activity was not ascertained because it was uncommonat the time of the baseline examination. Cigarette smoking wasdefined as smoking at least 1 cigarette per day for 1 yr. Datawere collected on the amount and the type of alcohol consumedduring the previous year.
Body weight and height were measured once during the visit bytrained observers using a standard protocol, and body mass index(BMI) was calculated as weight in kilograms divided by heightin meters squared. Overweight was defined in accordance withinternationally recognized definitions as a BMI 25.0 kg/m2 (13,14).Three BP measurements were obtained on a single occasion bytrained nurses or doctors according to a standard protocol thatwas adapted from procedures that are recommended by the AmericanHeart Association (15). BP was measured on the right arm inthe sitting position using a standardized mercury sphygmomanometerafter the participant had rested quietly for at least 5 min.In addition, participants were advised to avoid exercising;cigarette smoking; and consuming alcohol, coffee, or tea forat least 30 min before their BP measurement. The first and fifthKorotkoff sounds were recorded as SBP and DBP, respectively(15). The averages of all SBP and DBP measurements were usedto define SBP and DBP, respectively.
Follow-Up Data Collection
Follow-up interviews were conducted in 1999 and 2000 and includedtracking study participants or their proxies to a current address,performing in-depth interviews to ascertain disease status andvital information, and obtaining hospital records and deathcertificates. All ESRD events that were reported during thein-person/proxy interview were verified by obtaining medicalrecords or death certificates from the local hospital, dialysisunit, public health department, or police department. ESRD wasdefined as renal replacement therapy (dialysis or renal transplantation)or death from renal failure. Trained study staff visited allhospitals and dialysis units where patients received their treatment.The participants’ hospital records, including medicalhistory, physical examination findings, laboratory test results,discharge diagnosis, and/or autopsy findings were abstractedby study staff using a standard form. In addition, photocopiesof selected sections of the participants’ inpatient record,discharge summary, and pathology reports were obtained.
An end-point assessment committee in each province reviewedand confirmed (or rejected) the hospital’s discharge diagnosisand cause of death on the basis of the abstracted informationusing prespecified criteria. All completed abstraction formsof hospital records, death certificates, and photocopies ofhospital charts were sent to the Cardiovascular Institute ofthe Chinese Academy of Medical Sciences in Beijing, where astudy-wide end-point assessment committee independently reviewedall ESRD cases. Each ESRD case was verified by two committeemembers, the results were compared, and discrepancies were adjudicatedby discussion involving additional committee members. The underlyingcauses of ESRD were largely based on hospital discharge diagnosesthat were assigned by nephrologists or internists. Patients’hospital charts were reviewed to confirm a personal medicalhistory of diabetes, hypertension, glomerulonephritis, or othercauses for ESRD. Deaths were classified as being due to renalfailure when one of the following International Classificationof Diseases, 9th Revision, Clinical Modification codes was listedon the death certificate as the underlying cause: 403 to 404(hypertensive renal disease); 250.4 (diabetes mellitus withnephropathy); 274.1 (gouty nephropathy); 275.4 (nephrocalcinosis),593.3, 593.4, 593.5, 593.7, 593.8, 593.9 (other kidney disorders);596 (bladder-neck obstruction); 600 (hyperplasia of prostate);753.1 (cystic kidney disease); 580 to 589 (nephritis, nephriticsyndrome, or nephrosis); 590 (infection of the kidney); 591(hydronephrosis); and 592 (calculus of the kidney and ureter)(16).
This study was approved by the Tulane University Health SciencesCenter Institutional Review Board and the Cardiovascular Instituteand Fu Wai Hospital Ethics Committee. Written informed consentwas obtained from all study participants at their follow-upvisit.
Statistical Analyses
Study participants were grouped according to the Seventh Reportof the Joint National Committee on Prevention, Detection, Evaluation,and Treatment of High Blood Pressure (JNC-7) classificationof BP as measured at the baseline examination (normal BP: SBP<120 mmHg and DBP <80 mmHg; prehypertension: SBP between120 and 139 mmHg or DBP between 80 and 89 mmHg; stage 1 hypertension:SBP between 140 and 159 mmHg or DBP between 90 and 99 mmHg;and stage 2 hypertension: SBP 160 mmHg or DBP 100 mmHg) (17).Participants who reported current use of antihypertensive medicationwere included in the stage 2 hypertension category. Person-yearsof follow-up for each study participant were calculated fromthe date of the baseline examination until the date of death,development of ESRD, or the follow-up interview, whichever occurredfirst. Cumulative incidence of ESRD was calculated by JNC-7BP category using the Kaplan-Meier method with differences acrosscategories assessed using the log-rank test (18,19). Age-standardizedincidence rates were calculated by JNC-7 BP category using 5-yrage and gender-specific incidence rates and the age distributionof the Chinese population from year 2000 census data as thestandard.
Cox proportional hazards models were used to examine the multivariateadjusted relationship of BP categorized by JNC-7 with the incidenceof ESRD. Initial models included adjustment for age and gender.Subsequent models included additional adjustment for geographicregion (north versus south China), urbanization (urban versusrural residence), education, BMI, physical activity, currentcigarette smoking, alcohol drinking, and history of diabetesand cardiovascular disease (stroke or coronary heart disease).History of diabetes and cardiovascular disease was modeled asa time-dependent variable in extended Cox models (20). Theseanalyses were conducted separately for all-cause ESRD, glomerulonephritis-relatedESRD, non–glomerulonephritis-related ESRD, and unknowncause of ESRD. Population-attributable risks were calculatedfor each BP category (21).
To explore further the association of BP with ESRD, we determinedthe incidence and hazard ratios of ESRD for quintile of SBP(<108.5, 108.5 to 118.5, 118.5 to 128.5, 128.5 to 141, and141 mmHg), DBP (<68, 68 to 74, 74 to 80, 80 to 87, and 87mmHg), and pulse pressure (<37, 37 to 42.5, 42.5 to 50, 50to 60, and 60 mmHg). In addition, multivariate adjusted hazardratios that were associated with 1 SD higher BP were used tocompare the association of SBP, DBP, and pulse pressures withESRD. Analyses of BP as a continuous variable were performedwith each BP component included in the regression model separatelyand with both SBP and DBP simultaneously included in the regressionmodels (or, equivalently, both pulse pressure and SBP or pulsepressure and DBP). Methods that take into account the multistagesample clustering were used to estimate variance in the Coxproportional hazards models (22). Statistical analyses wereconducted using SAS statistical software (version 9.1; SAS Institute,Cary, NC).
Baseline characteristics of the study participants are presentedaccording to JNC-7 BP category in Table 1. Participants withhigher BP were older and more likely to be male, to live innorthern China and urban areas, to have a high school education,to drink alcohol, to be current smokers, to be physically inactive,to be overweight, and to have a history of stroke or coronaryheart disease.
Table 1. Baseline characteristics according to JNC-7 BP category in 158,365 CHEFS participants, China 1991 to 2000a
During an average follow-up of 8.3 yr (1,236,422 person-yearsof observation), 380 participants (30.7 cases per 100,000 person-years)initiated renal replacement therapy (n = 121) or died from renalfailure (n = 259). Glomerulonephritis was the most common underlyingassigned cause of ESRD (10.8 cases per 100,000 person-years)followed by diabetes (5.0 cases per 100,000 person-years) andhypertension (2.7 cases per 100,000 person-years; Table 2).
Table 2. Crude rates of ESRD in 158,365 CHEFS participants, China 1991 to 2000
The cumulative incidence of all-cause ESRD after 8 yr of follow-upwas 0.14, 0.23, 0.34, and 0.64% among participants with normalBP, prehypertension, stage 1 hypertension, and stage 2 hypertension,respectively (P < 0.001 trend; Figure 1).
Figure 1. Cumulative incidence of all-cause ESRD according to Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure (JNC-7) BP category among 158,365 China National Hypertension Survey Epidemiology Follow-Up Study (CHEFS) participants, China 1991 to 2000.
The association between BP and all-cause ESRD was positive andgraded after age, age–gender, and multivariate adjustment(Table 3). This association was consistent for glomerulonephritis-relatedESRD, non–glomerulonephritis-related ESRD, and ESRD fromunknown causes. Stage 1 and stage 2 hypertension were attributablefor 6.1 and 17.3% of all ESRD cases, respectively.
Table 3. Incidence rates and HR of ESRD by JNC-7 BP category in 158,365 CHEFS participants, China 1991 to 2000a
Higher quintile of systolic BP, diastolic BP, and pulse pressurewere each associated with an increased incidence and age-sexand multivariate adjusted hazard ratio of ESRD (Table 4). Themultivariate adjusted hazard ratio associated with a similarproportional increase in BP was greatest for systolic BP andlowest for diastolic BP. For example, compared with the lowestquintile, the multivariate-adjusted hazard ratio of ESRD forthe highest quintile of BP was 2.32 for systolic BP, 1.58 fordiastolic BP, and 2.05 for pulse pressure.
Table 4. Incidence rates and HR of all-cause ESRD according to quintiles of SBP, DBP, and pulse pressure in 158,365 CHEFS participants, China 1991 to 2000
The multivariate adjusted hazard ratio of all-cause ESRD associatedwith each 1-SD increase of BP (22.4 mmHg, SBP; 12.1 mmHg, DBP;16.1 mmHg, pulse pressure) was higher for SBP compared withDBP and pulse pressure (Table 5). In multivariate models thatincluded SBP and DBP simultaneously or included SBP and pulsepressure simultaneously, only SBP was significantly associatedwith an increased risk for all-cause ESRD. In a multivariatemodel that included DBP and pulse pressure simultaneously, bothpressures were associated with increased risk for all-causeESRD.
This study contributes to our knowledge of ESRD in China inseveral ways. First, our study documents an incidence rate forall-cause ESRD of 30.7 per 100,000 in Chinese men and womenwho are 40 yr and older. The burden of ESRD in China and othereconomically developing countries is largely unknown. Chinadoes not have a national registration system of ESRD, and previousreports reflected only information that was collected from selectedphysicians and hospitals. According to the Chinese Dialysisand Transplantation Registration Group and other hospital-basedstudies, ESRD incidence in China ranged from 1.5 to 14.8 per100,000 population (12,23,24). These low rates may reflect anincomplete ascertainment of ESRD cases. To the best of our knowledge,this study is the first to provide information on the incidenceof ESRD among a nationally representative sample of the adultpopulation in China.
Second, our study observed a strong, independent, and gradedassociation between BP and risk for all-cause ESRD and cause-specificESRD in the Chinese population. Only a few longitudinal studieshave examined the relationship of BP with the risk for ESRD(6–9). Klag et al. (6) identified a graded, continuous,and strong relationship between BP and risk for all-cause ESRDduring an average of 16 yr of follow-up among 332,544 middle-agedmen who had been screened for the Multiple Risk Factor InterventionTrial (MRFIT). More recently, Hsu et al. (9) reported similarfindings among 316,675 men and women who were members of KaiserPermanente in northern California and participated in healthcheck-ups between 1964 and 1985. Higher DBP was significantlyrelated with an increased risk for ESRD in 107,192 Japanesemen and women who were 18 yr or older and followed for 11 yr(25), and after 17 yr, both SBP and DBP were found to be independentrisk factors for ESRD (8). Perry et al. (7) found that SBP wasassociated with an increased risk of ESRD in 5730 black and6182 nonblack male veterans with hypertension.
Third, our study found that higher BP was associated with anincreased risk for glomerulonephritis-related and non–glomerulonephritis-relatedESRD. Participants with stage 2 hypertension had a 3.4-foldgreater risk for developing glomerulonephritis-related ESRDand 2.2-fold greater risk for developing non–glomerulonephritis-relatedESRD compared with their counterparts with normal BP. Previousprospective cohort studies have not reported on the associationbetween BP and glomerulonephritis-related ESRD (6–9).Glomerulonephritis is reported to be the primary cause of ESRDin China and other Asian populations (12,26). Our investigationprovides novel data that BP may be an important risk factorfor glomerulonephritis-related ESRD.
Fourth, our study indicated that SBP was a stronger predictorof all-cause ESRD than DBP or pulse pressure. In this study,SBP was a more potent predictor of ESRD than DBP or pulse pressure.The predictive power of SBP and DBP in relation to the riskfor ESRD was studied in men who were screened for the MRFITwith greater predictive power being noted for SBP (6). Younget al. (27) found that both SBP and pulse pressure were predictorsof a decline in kidney function (a rise in serum creatinine0.4 mg/dl) among older adults with isolated systolic hypertension.In that study, SBP had the greatest ability to predict a declinein kidney function.
Additional strengths of this study include the high follow-uprate over 8 yr and the use of stringent training and qualitycontrol processes, standard protocols, and criteria for assessingthe presence or absence of ESRD. Furthermore, this cohort provideda unique opportunity to study the relationship of BP with ESRDbecause of the wide range of BP and limited use of antihypertensivemedications. Only 2.8% of the study population was taking antihypertensivemedications at baseline, thereby limiting the potential forconfounding by treatment.
There are several potential limitations to this study. First,BP was measured three times on a single occasion. Because BPmeasurements are subject to random variation within person,use of a single-day baseline BP could have resulted in an underestimationof the association between usual BP and ESRD incidence (28).Second, baseline serum creatinine concentrations and urinaryprotein excretion were not measured. Furthermore, the baselinequestionnaire did not assess personal history of chronic kidneydisease. Consequently, it is unknown whether chronic kidneydisease was already present in those for whom ESRD subsequentlydeveloped. Therefore, our study cannot establish a causal relationshipbetween BP and ESRD. However, our investigation is a prospectivecohort study, and individuals with ESRD at baseline (those onrenal replacement therapy or with a kidney transplant) wereexcluded from the analysis. Finally, the cause of ESRD was notknown for a high proportion of the ESRD cases. Therefore, powerwas limited in ascertaining the association between elevatedBP levels and cause-specific ESRD.
These findings have important clinical and public health implications.Recent national data from China indicate that the prevalenceof hypertension increased 42% in men and 35% in women duringthe past decade (11). Moreover, only 8.1% of adults in Chinawith hypertension have their BP controlled to <140/90 mmHg(11). Our findings suggest that the prevention and control ofhypertension could reduce the incidence of ESRD by 23% in thegeneral population in China. Strategies that aim to preventESRD in China need to incorporate the prevention, treatment,and control of high BP.
This study was supported by a national Grant-in-Aid (9750612N)from the American Heart Association (Dallas, TX) and partiallysupported by a grant (U01 DK60963) from the National Instituteof Diabetes and Digestive and Kidney Diseases, the NationalInstitutes of Health (Bethesda, MD) and by a grant (1999-272)from the Chinese Ministry of Health (Beijing, China) and bythe Chinese Academy of Medical Sciences (Beijing, China). K.R.was partially supported by grant P20-RR17659 from the NationalCenter for Research Resources, a component of the National Institutesof Health.
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Published online ahead of print. Publication date availableat www.jasn.org.
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Abstract
Introduction
1 yr. Data were collected on the amount and the type of alcohol consumed during the previous year. 
