| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
(Circulation. 1999;99:2389-2395.)
© 1999 American Heart Association, Inc.
Clinical Investigation and Reports |
Rising Tide of Cardiovascular Disease in American Indians
The Strong Heart Study
From Medlantic Research Institute and Washington Hospital Center, Washington, DC (B.V.H., W.J.H., D.C.R., M.L.S.); Center for American Indian Health Research, University of Oklahoma Health Sciences Center, Oklahoma City (E.T.L., O.T.G.); the Department of Biostatistics and Epidemiology, University of Oklahoma, Oklahoma City (L.D.C.); Cornell University, College of Medicine, Ithaca, NY (R.B.D.); Center for Native American Health, Tucson, Ariz (J.M.G.); College of Medicine, University of Oklahoma, Oklahoma City (E.R.R); and Aberdeen Area Tribal Chairmen's Health Board, Rapid City, SD (T.K.W.).
Correspondence to Barbara V. Howard, PhD, Medlantic Research Institute, 108 Irving St, NW, Washington, DC 20010. E-mail bvh1{at}mhg.edu
 |
Abstract |
|---|
 Top Abstract IntroductionMethodsResultsDiscussionReferences |
|---|
Background—Although cardiovascular disease (CVD) used to be rare among American Indians, Indian Health Service data suggest that CVD mortality rates vary greatly among American Indian communities and appear to be increasing. The Strong Heart Study was initiated to investigate CVD and its risk factors in American Indians in 13 communities in Arizona, Oklahoma, and South/North Dakota.
Methods and Results—A total of 4549 participants (1846 men and 2703 women 45 to 74 years old) who were seen at the baseline (1989 to 1991) examination were subjected to surveillance (average 4.2 years, 1991 to 1995), and 88% of those remaining alive underwent a second examination (1993 to 1995). The medical records of all participants were exhaustively reviewed to ascertain nonfatal cardiovascular events that occurred since the baseline examination or to definitively determine cause of death. CVD morbidity and mortality rates were higher in men than in women and were similar in the 3 geographic areas. Coronary heart disease (CHD) incidence rates among American Indian men and women were almost 2-fold higher than those in the Atherosclerosis Risk in Communities Study. Significant independent predictors of CVD in women were diabetes, age, obesity (inverse), LDL cholesterol, albuminuria, triglycerides, and hypertension. In men, diabetes, age, LDL cholesterol, albuminuria, and hypertension were independent predictors of CVD.
Conclusions—At present, CHD rates in American Indians exceed rates in other US populations and may more often be fatal. Unlike other ethnic groups, American Indians appear to have an increasing incidence of CHD, possibly related to the high prevalence of diabetes. In the general US population, the rising prevalence of obesity and diabetes may reverse the decline in CVD death rates. Therefore, aggressive programs to control diabetes and its risk factors are needed.
Key Words: cardiovascular diseases • heart disease • mortality • Indians, North American • risk factors
|
Introduction |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
American Indians were long thought to have inherent protection from cardiovascular disease (CVD).1 A review of Indian Health Service (IHS) records from the 1960s showed very low rates,2 and coronary heart disease (CHD) mortality rates in Pima Indians from 1965 to 1980 were lower than those in the Framingham Study.3 More recent IHS data, however, indicate that CVD is now the leading cause of death among American Indians.4 5
Mortality data from 1980s IHS records also showed that CVD mortality rates varied: Some tribes had substantially higher (eg, the Northern Plains Indians) or lower (eg, Navaho, Pima) rates than those of the general US population.4 Interpretation of these data is difficult, however, because of the variation in quality of death certificate data and limitations in the determination of the population at risk. Moreover, American Indians have been undergoing rapid changes in lifestyle, with alterations in traditional patterns of activity and diet that might be expected to increase their risk of CVD. Furthermore, the prevalence of diabetes, a strong determinant of CVD, has been rising in American Indians.
The Strong Heart Study was initiated in 1988 to investigate CVD and its risk factors in geographically diverse groups of American Indians. Prevalence data from the initial examination suggested that American Indians had somewhat lower rates of myocardial infarction (MI) and CHD than other US groups2 6 and a lower prevalence of MI and CHD in certain Arizona Indians compared with those in South/North Dakota or Oklahoma. A 1984 to 1988 mortality survey, however, showed fewer differences in CVD mortality rates among geographic areas. CVD mortality rates in these tribal groups were somewhat higher than the respective state rates in Arizona and Oklahoma and almost 2 times higher than rates in South/North Dakota.7 These findings suggested that CVD incidence rates are increasing and that CVD more often may be fatal in American Indians. This report presents the results of a 7-year surveillance of CVD morbidity and mortality rates in the 4549 members of the original Strong Heart Study cohort and assesses the association of major risk factors with CVD incidence.
|
Methods |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
The study design, survey methods, and laboratory techniques of the Strong Heart Study have been reported previously.8 9 The study population included resident members of the following tribes: Pima/Maricopa/Papago Indians of central Arizona who live in the Gila River, Salt River, and Ak-Chin Indian communities; the 7 tribes of southwestern Oklahoma (Apache, Caddo, Comanche, Delaware, Fort Sill Apache, Kiowa, and Wichita); and the Oglala and Cheyenne River Sioux in South Dakota and the Spirit Lake Tribe in the Fort Totten area of North Dakota.
The study cohort consists of 4549 individuals aged 45 to 74 who were seen at the first (phase I) examination, conducted between July 1989 and January 1992. Participation rates of all age-eligible tribal members were 72% in the Arizona center, 62% in the Oklahoma center, and 55% in the South/North Dakota center.10 Nonparticipants were similar to participants in age and self-reported frequency of diabetes. Reexamination rates for those alive at the second (phase II) examination (July 1993 to December 1995) averaged 88%.
The phase I and phase II clinical examinations consisted of a personal interview and a physical examination. Fasting blood samples were obtained for measurements of lipids and lipoproteins, insulin, plasma creatinine, plasma fibrinogen, and glycohemoglobin, and a 75-g oral glucose tolerance test was performed as described previously.11 Laboratory methods were published previously.8 9
Weight, height, and waist and hip circumferences were measured and
percent body fat was estimated as described previously.8 9
Blood pressure measurements were obtained and
electrocardiograms were taken, read, and coded as
described previously.8 9 Percentage of Indian heritage was
computed from reported degree of Indian heritage for each parent and
grandparent. Participants were classified as diabetic according to
World Health Organization criteria.12 Participants were
considered hypertensive if they were taking antihypertension medication
or if they had a systolic blood pressure >140 mm Hg or a
diastolic blood pressure >90 mm Hg. Urinary
albumin excretion was estimated by the ratio of albumin
(mg) to creatinine (g). Microalbuminuria was
defined as a ratio of urinary albumin (mg/mL) to
creatinine (g/mL) of 30 to 299 mg/g and
macroalbuminuria as a ratio 
300 mg/g.
Deaths among the original Strong Heart Study cohort between the participants' first examination and December 1995 were identified through tribal and IHS hospital records and by direct contact by study personnel with participants and their families. Copies of death certificates were obtained from state health departments and ICD-9 coded centrally by a nosologist. Possible CVD deaths were initially identified from death certificates as described previously.7 Cause of death was investigated through autopsy reports, medical record abstractions, and informant interviews, as described previously.7 All materials were reviewed independently by physician members of the Strong Heart Study Mortality Review Committee to confirm the cause of death. Criteria for fatal CHD and stroke were as described previously.7
Medical records were reviewed at the second examination to identify any nonfatal cardiovascular events that had occurred since the phase I examination. Records of those who did not participate in the second examination (n=498; 2 died in 1996) also were reviewed. New MI and new CVD events were defined as in the first examination.2 For all potential CVD events or interventions, medical records were reviewed by trained medical record abstractors. Records of outpatient visits were reviewed and abstracted for procedures diagnostic of CVD (eg, treadmill tests, coronary angiography). Information obtained from the chart review was reviewed by a physician member of the Strong Heart Study mortality or morbidity review committee to establish the specific CVD diagnosis. Blinded review of the abstracted records by other physician members of the Morbidity Review Committee showed >90% concordance in diagnosis.
Data Analysis
Incidence rates for fatal and nonfatal events were calculated
per 1000 person-years after elimination of individuals in the cohort
who had definite CHD or stroke at baseline. Person-years were
calculated from the date of the phase I examination to diagnosis or
time of the first event. Statistical significance of center-specific
differences was evaluated by 
2
test.13 Univariate assessment of associations
of risk factors at baseline with incident CVD was performed by
univariate logistic regression analysis, adjusted
for age and center, in those with and those without events. A Cox
proportional hazards model was used for computing age- and
center-adjusted hazard rate ratios and 95% confidence intervals. All
variables examined in the univariate analyses,
plus sex and center, were then used in the model for examination of CVD
risk factors. Stepwise Cox regression analysis, with entry and
retention criteria of 5%, was used to compute hazard rate ratios for
the multivariate analysis.
|
Results |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
The population at risk for CVD mortality or morbidity in the follow-up interval (7 years; average 4.2 years) was 4380 individuals (Table 1
). In both women and men,
CHD mortality rates (Table 2) did not
differ significantly between centers. In all 3 centers, fatal CHD rates
were significantly higher in men than in women (P<0.0001).
Rates for fatal stroke were lower than those for fatal CHD. Rates for
fatal stroke did not differ significantly between centers.
|
|
Incidence rates for nonfatal CVD (Table 3) were similar for nonfatal CHD in
Arizona and South/North Dakota women, with rates in Oklahoma women
being somewhat but not significantly lower. Among men, rates for
nonfatal CHD were highest in South/North Dakota and lowest in Arizona
(P=0.17). In all 3 centers, rates for nonfatal CHD were
higher among men than among women (P<0.01). As was observed
for fatal stroke, rates for nonfatal stroke were much lower than for
nonfatal CHD. Rates for nonfatal stroke were somewhat but not
significantly higher among both men and women in South/North Dakota
compared with the other 2 centers. In all 3 centers, rates for nonfatal
stroke were similar in men and women.
|
Figure 1 shows composite incidence rates
of CVD (morbidity plus mortality) in men and women in the three
geographic areas. In men, combined rates were lowest in Arizona,
highest in South/North Dakota, and intermediate in Oklahoma
(P=0.09). In women, the combined rates also were highest in
South/North Dakota but lowest in Oklahoma (P=0.11). The
differences in men are largely due to differences in nonfatal events,
with mortality rates being very similar in all 3 centers.
|
Major risk factors for fatal and nonfatal CVD were evaluated with the
use of Cox regression analysis, adjusting for age and center
(Table 4). Hypertension, HDL
cholesterol (inverse), albuminuria, and
fibrinogen were each associated with CVD in both men and women.
Diabetes was strongly associated with disease in both men and women,
with diabetic men having a 2.2-fold increased risk of CVD and diabetic
women having a 3.5-fold increased rate compared with nondiabetic
individuals. The other strong risk factor in both sexes was
albuminuria, with men with macroalbuminuria
having a 3.8-fold increase in CVD risk and women with
macroalbuminuria having a 5.4-fold increase in risk. LDL
cholesterol was a significant predictor in men but not in
women. Obesity, as measured by percent body fat, was a significant
inverse predictor in women but not in men, and body fat distribution,
determined by waist circumference, was not related to CVD in either
sex. Triglyceride concentration was a significant predictor
in women but not in men. Insulin concentration was a significant
predictor in men but not in women. When full-blooded Indians were
compared with those with non-Indian admixture, there was no association
with CVD risk. There was no association between smoking and CVD in
either men or women.
|
In a multivariate stepwise Cox proportional hazards
analysis (Table 5), the
significant independent predictors of CVD in women were
albuminuria, age, diabetes, obesity (inverse), LDL
cholesterol, triglycerides, and hypertension.
In men, age, albuminuria, LDL cholesterol,
diabetes, and hypertension were independent predictors.
|
CVD rates in the Strong Heart Study were compared with other US
populations (Figure 2), as
measured by the Cardiovascular Health Study
(CHS)14 and the Atherosclerosis Risk in
Communities (ARIC) Study,15 which used similar methods of
ascertainment. Rates for stroke are similar in women and lower in
American Indian men than in the general US population, but rates for
CHD in American Indian men and women are almost 2-fold higher than the
US population.
|
|
Discussion |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
The present longitudinal analysis was undertaken to clarify the apparent discrepancy between the initial cross-sectional data2 6 and subsequent reports7 on CVD prevalence and mortality in the Strong Heart Study. The present data showed that whereas incidence rates for nonfatal CVD in Arizona men were lower than those in Oklahoma and South/North Dakota, incidence rates for nonfatal CVD in women and CVD mortality in both men and women were similar in all 3 centers.
The present CVD incidence data were compared with those in the
CHS14 and ARIC15 studies: 2 other national
population studies with predominantly white (CHS) and 25% black (ARIC)
cohorts (Figure 2
). Rates for stroke in American Indians appear
to be lower for men than in the CHS data but similar for women; rates
for CHD in American Indian men and women, however, are almost 2-fold
higher than rates in the ARIC Study. These data suggest that rates of
coronary disease in American Indians may exceed those of other
US populations. In contrast to reports of low CVD rates from earlier
data1 3 16 and contrary to other US ethnic groups,
American Indians have rates of CVD that appear to be rising. Further,
coronary events may be more often fatal, especially in the
Arizona communities, as shown by their similar CVD death rates in men
despite lower incidence of nonfatal CVD events.
The most likely explanation for the high rates of CVD in American Indians is the high prevalence of diabetes in these communities. Univariate and multivariate analyses show that diabetes was the strongest determinant of CVD, with 56% of the events in men and 78% of the events in women occurring in those with diabetes. Because 70% of the individuals in Arizona and >40% in the other 2 centers had diabetes, diabetes thus accounts for an extremely high percentage of the population-attributable risk. Although diabetes is well known to increase CVD risk factors, the present analysis, as well as many others, shows a strong independent effect of diabetes after adjustment for other risk factors.
Hyperglycemia may contribute to atherosclerosis by impeding endothelial function17 18 and causing advanced glycation end products to form that may promote myocardial dysfunction. This latter effect has been demonstrated in Strong Heart Study echocardiograms that show increases in left ventricular wall thickness and mass, ventricular dysfunction, and evidence of increased arterial stiffness in individuals with diabetes.19
Albuminuria was one of the strongest correlates of CVD both in this longitudinal analysis and the baseline cross-sectional data. Several prospective studies examining risk factors for CVD among individuals with diabetes have observed a relation between albuminuria and CVD.20 21 22 Renal disease may be related to CVD because of its influence on lipoproteins, blood pressure, and other metabolic factors. Albuminuria remains a significant correlate in the multivariate analysis after adjustment for these factors as well as for the presence of diabetes. This suggests that the association between diabetes and CHD may share common determinants with microvascular disease in other organs, of which albuminuria is a marker. Thus microvascular disease is the probable cause of the renal disease, left ventricular dysfunction, and other echocardiographic abnormalities that we have documented in diabetic Strong Heart Study participants. The consistent finding of albuminuria as a major risk factor further emphasizes the importance of measuring urinary albumin in clinical assessments of individuals with diabetes and applying aggressive measures to attempt to retard the progression of microvascular disease as a strategy to control coronary disease.
LDL cholesterol was a significant independent predictor of CVD in American Indian men and women. Total and LDL cholesterol levels in American Indians are lower than the US average,16 and this observation has impeded recognition of the potential importance of LDL cholesterol as a cause of coronary disease. The positive relation observed in this study shows that aggressive cholesterol lowering might lower CHD risk and supports the recently suggested target LDL levels of <100 mg/dL (<2.6 mmol/L) for individuals with diabetes.
Hypertension also was shown to be a predictor of coronary disease. Hypertension is common in American Indian communities except for South/North Dakota, and its prevalence is greater than in the general US population.23
American Indians and most individuals with diabetes have a high prevalence of the insulin resistance syndrome, which is a strong predictor of CHD. The Strong Heart Study data showed high insulin concentrations, high waist-hip ratios, and the typical dyslipidemia characterized by elevated triglycerides; low HDL; and small, dense LDL particles.6 24 In the present data, the univariate analysis showed that plasma insulin concentration was a significant correlate in men, triglycerides were significant in women, and HDL had a strong inverse association in both men and women. In the proportional hazards model, neither insulin nor HDL remained significant, and triglyceride was a significant predictor only in women. In this population, the very high prevalence of diabetes and renal disease may overshadow the atherogenic effects of insulin resistance per se, although the insulin resistance undoubtedly was a strong predisposing factor for the high rate of diabetes.
Rates of smoking are high in many American Indian communities, although numbers of cigarettes smoked per day are less than the US average.16 Although smoking was not a significant independent predictor of CHD, it has been shown to be a significant independent correlate of peripheral vascular disease in American Indians.25
Obesity had a negative association with CVD in both men and women, which was significant in both analyses in women. Body fat distribution showed no relation to CVD in women or men, probably because among obese American Indians, body fat almost always is centrally distributed. On the other hand, it is very difficult to understand the negative relation of obesity with CHD. It is possible that this reflects the fact that individuals with a long duration of diabetes, particularly those with renal disease (who are at high risk for CVD), lose weight, and that this is not completely accounted for in the multivariate analysis. The question of whether there may be ethnic differences in the impact of obesity on CVD needs further investigation.
The prospective surveillance of the Strong Heart Study cohort has
shown that incidence rates of fatal CVD in Arizona are actually higher
than those in Oklahoma and 
75% of those in South and North Dakota:
thus the demise of the "Pima Paradox," ie, the low prevalence and
mortality rates of coronary disease documented in earlier
studies of Arizona Indians.1 3 This is not surprising,
given the very high prevalence rates of diabetes in these communities
and the existence of several other risk factors such as hypertension
and albuminuria. Thus even in populations that may have had
innate protection or a lower tendency for
atherosclerosis, this protection can be overcome or
overridden by diabetes, its associated metabolic
abnormalities, and other CVD risk factors. It is entirely possible that
similar findings will be observed in other populations throughout the
world with traditionally low rates of coronary disease in whom
diabetes prevalence is increasing. Further, the rising prevalence of
obesity and consequently of diabetes in the general US population may,
in the future, lead to rising rates of CVD in the US population.
Diabetes prevention programs, coupled with programs aimed at aggressive
control of risk factors in diabetic individuals, may help to stem this
rising tide of diabetes-associated CHD in American Indians and in other
populations with increasing prevalence of diabetes.
|
Acknowledgments |
|---|
This study was supported by cooperative agreement grants (No. U01-HL-41642, U01HL-41652, and UL01HL-41654) from the National Heart, Lung, and Blood Institute. The authors acknowledge the assistance and cooperation of the AkChin Tohono O'Odham (Papago)/Pima, Apache, Caddo, Cheyenne River Sioux, Comanche, Delaware, Spirit Lake Tribe, Fort Sill Apache, Gila River, Pima/Maricopa, Kiowa, Oglala Sioux, Salt River Pima/Maricopa and Wichita Indian communities, without whose support this study would not have been possible. The authors also wish to thank the Indian Health Service hospitals and clinics at each center, and Betty Jarvis, Taqueer Ali, and Alan Crawford, directors of the Strong Heart Study clinics and their staffs; and the physicians who performed the morbidity and mortality reviews: R. Stuart Gray, Dorothy Rhoades, Sabeeh Jaffrey, Cheryl Pegas, Kamran Rafiq, Boureima Sambo, and Arvo Oopik, who died in a plane crash on February 22, 1994, while serving American Indian patients. We also acknowledge the editorial assistance of Ellen Shair.
|
Footnotes |
|---|
The views expressed in this report are those of the authors and do not necessarily reflect those of the Indian Health Service.
Received June 15, 1998; revision received February 3, 1999; accepted February 16, 1999.
|
References |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
1. Sievers ML, Fisher JR. Diseases of North American Indians. In: Rothschild HR, ed. Biocultural Aspects of Disease. New York, NY: Academic Press; 1981:191–252.
2.
Howard BV, Lee ET, Cowan LD, Fabsitz RR, Howard WJ,
Oopik AJ, Robbins DC, Savage PJ, Yeh JL, Welty TK. Coronary
heart disease prevalence and its relation to risk factors in American
Indians: the Strong Heart Study. Am J Epidemiol. 1995;142:254–268.
3.
Nelson RG, Sievers ML, Knowler WC, Swinburn BA,
Pettitt DJ, Saad MF, Liebow IM, Howard BV, Bennett PH. Low incidence of
fatal coronary heart disease in Pima Indians despite high
prevalence of non–insulin-dependent diabetes. Circulation. 1990;81:987–995.
4. Indian Health Service. IHS Chart Series Book, June 1984. Washington DC; US Government Printing Office, US Department of Health and Human Services.
5. US Congress. Office of Technology Assessment. Indian Health Care. OTA-H-290 (Washington, DC, US Government Printing Office, April 1986).
6. Oopik AJ, Dorogy M, Devereux RB, Yeh JL, Okin PM, Lee ET, Cowan L, Fabsitz RR, Howard BV, Welty TK. Major electrocardiographic abnormalities among American Indians aged 45 to 74 years (the Strong Heart Study). Am J Cardiol. 1996;78:1400–1405.[Medline] [Order article via Infotrieve]
7.
Lee ET, Cowan LD, Howard WJ, Sievers M, Welty TK, Wang
W, Yeh, JL, Rhoades ER, Devereux RB, Fabsitz RR, Go O, Howard BV.
All-cause mortality and cardiovascular disease
mortality in 3 American Indian populations aged 45 to 74 years, 1984 to
88: the Strong Heart Study. Am J Epidemiol. 1998;147:995–1008.
8.
Lee ET, Welty TK, Fabsitz R, Cowan LD, Lee N-A, Oopik
AJ, Cucchiara AJ, Savage PJ, Howard BV. The Strong Heart Study: a study
of cardiovascular disease in American Indians: design
and methods. Am J Epidemiol. 1990;132:1141–1155.
9. Howard BV, Welty TK, Fabsitz RR, Cowan LD, Oopik AJ, Le NA, Yeh J, Savage PJ, Lee ET. Risk factors for coronary heart disease in diabetic and nondiabetic Native Americans: the Strong Heart Study. Diabetes. 1992;41(suppl 2):4–11.
10. Stoddart M, Jarvis B, Blake B,, Fabsitz RR, Welty TK, Lee ET, Howard BV. Recruitment of American Indians in epidemiologic research: the Strong Heart Study. J Natl Center Am Indian Alaska Native Ment Health Res. In press.
11. Lee ET, Howard BV, Savage PJ, Cowan LD, Fabsitz RR, Oopik AJ, Yeh JL, Go O, Robbins DC, Welty TK. Diabetes and impaired glucose tolerance in 3 American Indian populations aged 45 to 74 years: the Strong Heart Study. Diabetes Care.. 1995;18:599–610.[Abstract]
12. WHO Expert Committee on Diabetes Mellitus. Second Report. Geneva, World Health Organization. 1980 (Technical Report Series 646).
13. Rothman KJ. Modern Epidemiology. Boston, Mass: Little, Brown & Co; 1986.
14.
Manolio TA, Kronmal RA, Burke GL, O'Leary DH, Price
TR. Short-term predictors of incident stroke in older adults: the
Cardiovascular Health Study. Stroke. 1996;27:1479–1486.
15.
Chambless LE, Heiss G, Folsom AR, Rosamond W, Szklo M,
Sharrett AR, Clegg LX. Association of coronary heart disease
incidence with carotid arterial wall thickness and major
risk factors: the Atherosclerosis Risk in Communities
(ARIC) Study, 1987 to 1993. Am J Epidemiol. 1997;146:483–494.
16.
Welty TK, Lee ET, Yeh J, Cowan LD, Fabsitz RR, Le NA,
Robbins DC, Oopik AJ, Howard BV. Cardiovascular disease
risk factors among American Indians: the Strong Heart Study.
Am J Epidemiol. 1995;142:269–287.
17.
Makimattila S, Virkamaki A, Gropp PH, Cockcraft J,
Utrianen T, Fagerudd J, Yki-Jarvinen H. Chronic hyperglycemia impairs
endothelial function and insulin sensitivity via
different mechanisms in insulin-dependent diabetes mellitus.
Circulation. 1996;94:1276–1282.
18. Yki-Jarvinen H, Makimattila S. Insulin resistance due to hyperglycaemia: an adaptation protecting insulin-sensitive tissues. Diabetologia. 1997;40(suppl 2):S141–S144.
19. Devereux RB, Roman MJ, Ilercil A, Paranicas M, O'Grady MJ, Welty TK, Fabsitz RR, Howard BV, Lee ET. Impact of diabetes on cardiac structure and function in American Indians: the Strong Heart Study. J Am Coll Cardiol. 1997;29:448A. Abstract.
20. Borch-Johnsen K, Kreiner S. Proteinuria. Value as a predictor of cardiovascular mortality in insulin-dependent diabetes mellitus. Br Med J. 1987;294:1651–1654.
21. Parving HH, Gall MA, Nielsen FS. Dyslipidaemia and cardiovascular disease in non-insulin-dependent diabetic patients with and without diabetic nephropathy. J Int Med. 1994;736:89–94.
22. Savage S, Estacio RO, Jeffers B, Schrier RW. Urinary albumin excretion as a predictor of diabetic retinopathy, neuropathy, and cardiovascular disease in NIDDM. Diabetes Care. 1996;19:1243–1248.[Abstract]
23.
Howard BV, Lee ET, Yeh JL, Go O, Fabsitz RR, Devereux
RB, Welty TK. Hypertension in adult American Indians: the Strong Heart
Study. Hypertension. 1996;28:256–264.
24.
Gray RS, Robbins DC, Wang W, Yeh JL, Fabsitz RR, Cowan
LD, Welty TK, Lee ET, Krauss RM, Howard BV. Relation of LDL size to the
insulin resistance syndrome and coronary heart disease in
American Indians: the Strong Heart Study. Arterioscler Thromb
Vasc Biol. 1997;17:2713–2720.
25.
Fabsitz RR, Sidawy AN, Go O, Lee ET, Welty TK, Devereux
RB, Howard BV. Prevalence of peripheral
arterial disease and associated risk factors in American
Indians: the Strong Heart Study. Am J Epidemiol.. 1999;149:330–338.
This article has been cited by other articles:
 |
|
 |
|
  L.-M. Baldwin, D. C. Grossman, E. Murowchick, E. H. Larson, W. B. Hollow, J. R. Sugarman, W. L. Freeman, and L. G. Hart Trends in Perinatal and Infant Health Disparities Between Rural American Indians and Alaska Natives and Rural Whites Am J Public Health, April 1, 2009; 99(4): 638 - 646. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. L. Fleg, M. Mete, B. V. Howard, J. G. Umans, M. J. Roman, R. E. Ratner, A. Silverman, J. M. Galloway, J. A. Henderson, M. R. Weir, et al. Effect of Statins Alone Versus Statins Plus Ezetimibe on Carotid Atherosclerosis in Type 2 Diabetes: The SANDS (Stop Atherosclerosis in Native Diabetics Study) Trial J. Am. Coll. Cardiol., December 16, 2008; 52(25): 2198 - 2205. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. R. Williams Racial/Ethnic Variations in Women's Health: The Social Embeddedness of Health Am J Public Health, September 1, 2008; 98(Supplement_1): S38 - S47. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. V. Howard, M. J. Roman, R. B. Devereux, J. L. Fleg, J. M. Galloway, J. A. Henderson, Wm. J. Howard, E. T. Lee, M. Mete, B. Poolaw, et al. Effect of Lower Targets for Blood Pressure and LDL Cholesterol on Atherosclerosis in Diabetes: The SANDS Randomized Trial JAMA, April 9, 2008; 299(14): 1678 - 1689. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. J. Shaw, R. E. Shaw, C. N. B. Merz, R. G. Brindis, L. W. Klein, B. Nallamothu, P. S. Douglas, R. J. Krone, C. R. McKay, P. C. Block, et al. Impact of Ethnicity and Gender Differences on Angiographic Coronary Artery Disease Prevalence and In-Hospital Mortality in the American College of Cardiology-National Cardiovascular Data Registry Circulation, April 8, 2008; 117(14): 1787 - 1801. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Cicala, G. de Simone, M. J. Roman, L. G. Best, E. T. Lee, W. Wang, T. K. Welty, J. M. Galloway, B. V. Howard, and R. B. Devereux Prevalence and Prognostic Significance of Wall-Motion Abnormalities in Adults Without Clinically Recognized Cardiovascular Disease: The Strong Heart Study Circulation, July 10, 2007; 116(2): 143 - 150. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. de Simone, R. B. Devereux, M. Chinali, L. G. Best, E. T. Lee, J. M. Galloway, H. E. Resnick, and for the Strong Heart Study Investigators Prognostic Impact of Metabolic Syndrome by Different Definitions in a Population With High Prevalence of Obesity and Diabetes: The Strong Heart Study Diabetes Care, July 1, 2007; 30(7): 1851 - 1856. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. J. Roman, R. B. Devereux, J. R. Kizer, E. T. Lee, J. M. Galloway, T. Ali, J. G. Umans, and B. V. Howard Central Pressure More Strongly Relates to Vascular Disease and Outcome Than Does Brachial Pressure: The Strong Heart Study Hypertension, July 1, 2007; 50(1): 197 - 203. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. E. Dixon, F. Yeh, T. K. Welty, E. R. Rhoades, E. T. Lee, B. V. Howard, P. L. Enright, and for the Strong Heart Study Research Group Asthma in American Indian Adults: The Strong Heart Study Chest, May 1, 2007; 131(5): 1323 - 1330. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Scavini, C. A. Stidley, S. S. Paine, V. O. Shah, F. Tentori, A. Bobelu, T. K. Welty, J. W. MacCluer, and P. G. Zager The Burden of Chronic Kidney Disease among the Zuni Indians: The Zuni Kidney Project Clin. J. Am. Soc. Nephrol., May 1, 2007; 2(3): 509 - 516. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Compher The Nutrition Transition in American Indians J Transcult Nurs, July 1, 2006; 17(3): 217 - 223. [Abstract] [PDF]
|
|
|
|
|
|
K. M. Conti Diabetes Prevention in Indian Country: Developing Nutrition Models to Tell the Story of Food-System Change J Transcult Nurs, July 1, 2006; 17(3): 234 - 245. [Abstract] [PDF]
|
|
|
|
|
|
E. T. Lee, B. V. Howard, W. Wang, T. K. Welty, J. M. Galloway, L. G. Best, R. R. Fabsitz, Y. Zhang, J. Yeh, and R. B. Devereux Prediction of Coronary Heart Disease in a Population With High Prevalence of Diabetes and Albuminuria: The Strong Heart Study Circulation, June 27, 2006; 113(25): 2897 - 2905. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. M. Okin, R. B. Devereux, E. Gerdts, S. M. Snapinn, K. E. Harris, S. Jern, S. E. Kjeldsen, S. Julius, J. M. Edelman, L. H. Lindholm, et al. Impact of Diabetes Mellitus on Regression of Electrocardiographic Left Ventricular Hypertrophy and the Prediction of Outcome During Antihypertensive Therapy: The Losartan Intervention For Endpoint (LIFE) Reduction in Hypertension Study Circulation, March 28, 2006; 113(12): 1588 - 1596. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. Wang, E. T. Lee, R. R. Fabsitz, R. Devereux, L. Best, T. K. Welty, and B. V. Howard A Longitudinal Study of Hypertension Risk Factors and Their Relation to Cardiovascular Disease: The Strong Heart Study Hypertension, March 1, 2006; 47(3): 403 - 409. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. V. Howard, L. G. Best, J. M. Galloway, W. J. Howard, K. Jones, E. T. Lee, R. E. Ratner, H. E. Resnick, and R. B. Devereux Coronary Heart Disease Risk Equivalence in Diabetes Depends on Concomitant Risk Factors Diabetes Care, February 1, 2006; 29(2): 391 - 397. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. A. Rhoades National Health Data and Older American Indians and Alaska Natives Journal of Applied Gerontology, February 1, 2006; 25(1_suppl): 9S - 26S. [Abstract] [PDF]
|
|
|
|
|
|
G. de Simone, R. B. Devereux, M. Chinali, M. J. Roman, L. G. Best, T. K. Welty, E. T. Lee, B. V. Howard, and for the Strong Heart Study Investigators Risk Factors for Arterial Hypertension in Adults With Initial Optimal Blood Pressure: The Strong Heart Study Hypertension, February 1, 2006; 47(2): 162 - 167. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. S. Burnett, J. M. Devaney, R. J. Adenika, R. Lindsay, and B. V. Howard Cross-Sectional Associations of Resistin, Coronary Heart Disease, and Insulin Resistance J. Clin. Endocrinol. Metab., January 1, 2006; 91(1): 64 - 68. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Bullock and R. A. Bell STRESS, TRAUMA, AND CORONARY HEART DISEASE AMONG NATIVE AMERICANS Am J Public Health, December 1, 2005; 95(12): 2122 - 2123. [Full Text] [PDF]
|
|
|
|
 |
|
 R. T. Goins, S. M. Spencer, Y. D. Roubideaux, and S. M. Manson Differences in Functional Disability of Rural American Indian and White Older Adults With Comorbid Diabetes Research on Aging, November 1, 2005; 27(6): 643 - 658. [Abstract] [PDF]
|
|
|
|
 |
|
 R. Retnakaran, A. J.G. Hanley, P. W. Connelly, S. B. Harris, and B. Zinman Cigarette smoking and cardiovascular risk factors among Aboriginal Canadian youths Can. Med. Assoc. J., October 11, 2005; 173(8): 885 - 889. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. S. Harwell, C. S. Oser, N. J. Okon, C. C. Fogle, S. D. Helgerson, and D. Gohdes Defining Disparities in Cardiovascular Disease for American Indians: Trends in Heart Disease and Stroke Mortality Among American Indians and Whites in Montana, 1991 to 2000 Circulation, October 11, 2005; 112(15): 2263 - 2267. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Wilson, S. Gilliland, T. Cullen, K. Moore, Y. Roubideaux, L. Valdez, W. Vanderwagen, and K. Acton Diabetes Outcomes in the Indian Health System During the Era of the Special Diabetes Program for Indians and the Government Performance and Results Act Am J Public Health, September 1, 2005; 95(9): 1518 - 1522. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. G. Best, Y. Zhang, E. T. Lee, J.-L. Yeh, L. Cowan, V. Palmieri, M. Roman, R. B. Devereux, R. R. Fabsitz, R. P. Tracy, et al. C-Reactive Protein as a Predictor of Cardiovascular Risk in a Population With a High Prevalence of Diabetes: The Strong Heart Study Circulation, August 30, 2005; 112(9): 1289 - 1295. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Lamon-Fava, J. B. Barnett, M. N. Woods, C. McCormack, J. R. McNamara, E. J. Schaefer, C. Longcope, B. Rosner, and S. L. Gorbach Differences in Serum Sex Hormone and Plasma Lipid Levels in Caucasian and African-American Premenopausal Women J. Clin. Endocrinol. Metab., August 1, 2005; 90(8): 4516 - 4520. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. H. Denny, D. Holtzman, R. T. Goins, and J. B. Croft Disparities in Chronic Disease Risk Factors and Health Status Between American Indian/Alaska Native and White Elders: Findings From a Telephone Survey, 2001 and 2002 Am J Public Health, May 1, 2005; 95(5): 825 - 827. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. R. Burrows, A. S. Narva, L. S. Geiss, M. M. Engelgau, and K. J. Acton End-Stage Renal Disease due to Diabetes Among Southwestern American Indians, 1990-2001 Diabetes Care, May 1, 2005; 28(5): 1041 - 1044. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Fredy, D. A Diggins Jr, and G. B Morrill Blood Pressure in Native Americans Switched from Celecoxib to Rofecoxib Ann. Pharmacother., May 1, 2005; 39(5): 797 - 802. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. A. Rhoades Racial Misclassification and Disparities in Cardiovascular Disease Among American Indians and Alaska Natives Circulation, March 15, 2005; 111(10): 1250 - 1256. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. J. Benjamin, M. Jessup, J. M. Flack, H. M. Krumholz, K. Liu, V. M. Nadkarni, D. A. Rhoades, B. L. Rodriguez, R. P. Scott, M. P. Taylor, et al. Discovering the Full Spectrum of Cardiovascular Disease: Minority Health Summit 2003: Report of the Outcomes Writing Group Circulation, March 15, 2005; 111(10): e124 - e133. [Full Text] [PDF]
|
|
|
|
|
|
S. C. Smith Jr, L. T. Clark, R. S. Cooper, S. R. Daniels, S. K. Kumanyika, E. Ofili, M. A. Quinones, E. J. Sanchez, E. Saunders, and S. D. Tiukinhoy Discovering the Full Spectrum of Cardiovascular Disease: Minority Health Summit 2003: Report of the Obesity, Metabolic Syndrome, and Hypertension Writing Group Circulation, March 15, 2005; 111(10): e134 - e139. [Full Text] [PDF]
|
|
|
|
 |
|
 R. S. Lindsay, H. E. Resnick, J. Zhu, M. L. Tun, B. V. Howard, Y. Zhang, J. Yeh, and L. G. Best Adiponectin and Coronary Heart Disease: The Strong Heart Study Arterioscler. Thromb. Vasc. Biol., March 1, 2005; 25(3): e15 - e16. [Full Text] [PDF]
|
|
|
|
|
|
M. E. Pavkov, M. L. Sievers, W. C. Knowler, P. H. Bennett, and R. G. Nelson An Explanation for the Increase in Heart Disease Mortality Rates in Diabetic Pima Indians: Effect of renal replacement therapy Diabetes Care, May 1, 2004; 27(5): 1132 - 1136. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. E. Resnick, R. S. Lindsay, M. M. McDermott, R. B. Devereux, K. L. Jones, R. R. Fabsitz, and B. V. Howard Relationship of High and Low Ankle Brachial Index to All-Cause and Cardiovascular Disease Mortality: The Strong Heart Study Circulation, February 17, 2004; 109(6): 733 - 739. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. G. Best, M. Davidson, K. E. North, J. W. MacCluer, Y. Zhang, E. T. Lee, B. V. Howard, S. DeCroo, and R. E. Ferrell Prospective Analysis of Mannose-Binding Lectin Genotypes and Coronary Artery Disease in American Indians: The Strong Heart Study Circulation, February 3, 2004; 109(4): 471 - 475. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. M. Okin, R. B. Devereux, E. T. Lee, J. M. Galloway, and B. V. Howard Electrocardiographic Repolarization Complexity and Abnormality Predict All-Cause and Cardiovascular Mortality in Diabetes: The Strong Heart Study Diabetes, February 1, 2004; 53(2): 434 - 440. [Abstract] [Full Text]
|
|
|
|
|
|
V. Palmieri, R. P. Tracy, M. J. Roman, J. E. Liu, L. G. Best, J. N. Bella, D. C. Robbins, B. V. Howard, and R. B. Devereux Relation of Left Ventricular Hypertrophy to Inflammation and Albuminuria in Adults With Type 2 Diabetes: The Strong Heart Study Diabetes Care, October 1, 2003; 26(10): 2764 - 2769. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Roguin, W. Koch, A. Kastrati, D. Aronson, A. Schomig, and A. P. Levy Haptoglobin Genotype Is Predictive of Major Adverse Cardiac Events in the 1-Year Period After Percutaneous Transluminal Coronary Angioplasty in Individuals With Diabetes Diabetes Care, September 1, 2003; 26(9): 2628 - 2631. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. R. Rhoades The Health Status of American Indian and Alaska Native Males Am J Public Health, May 1, 2003; 93(5): 774 - 778. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. E. Resnick, K. Jones, G. Ruotolo, A. K. Jain, J. Henderson, W. Lu, and B. V. Howard Insulin Resistance, the Metabolic Syndrome, and Risk of Incident Cardiovascular Disease in Nondiabetic American Indians: The Strong Heart Study Diabetes Care, March 1, 2003; 26(3): 861 - 867. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. E. North, B. V. Howard, T. K. Welty, L. G. Best, E. T. Lee, J. L. Yeh, R. R. Fabsitz, M. J. Roman, and J. W. MacCluer Genetic and Environmental Contributions to Cardiovascular Disease Risk in American Indians: The Strong Heart Family Study Am. J. Epidemiol., February 15, 2003; 157(4): 303 - 314. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. Lu, H. E. Resnick, K. A. Jablonski, K. L. Jones, A. K. Jain, Wm. J. Howard, D. C. Robbins, and B. V. Howard Non-HDL Cholesterol as a Predictor of Cardiovascular Disease in Type 2 Diabetes: The Strong Heart Study Diabetes Care, January 1, 2003; 26(1): 16 - 23. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. P. Levy, I. Hochberg, K. Jablonski, H. E. Resnick, E. T. Lee, L. Best, and B. V. Howard Haptoglobin phenotype is an independent risk factor for cardiovascular disease in individuals with diabetes: the strong heart study J. Am. Coll. Cardiol., December 4, 2002; 40(11): 1984 - 1990. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. E. Resnick Metabolic Syndrome in American Indians Diabetes Care, July 1, 2002; 25(7): 1246 - 1247. [Full Text] [PDF]
|
|
|
|
 |
|
 J. L. Sewell, B. R. Malasky, C. L. Gedney, T. M. Gerber, E. A. Brody, E. A. Pacheco, D. Yost, B. R. Masden, and J. M. Galloway The Increasing Incidence of Coronary Artery Disease and Cardiovascular Risk Factors Among a Southwest Native American Tribe: The White Mountain Apache Heart Study Arch Intern Med, June 24, 2002; 162(12): 1368 - 1372. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. V. Howard, B. L. Rodriguez, P. H. Bennett, M. I. Harris, R. Hamman, L. H. Kuller, T. A. Pearson, and J. Wylie-Rosett Prevention Conference VI: Diabetes and Cardiovascular Disease: Writing Group I: Epidemiology Circulation, May 7, 2002; 105 (18): e132 - e137. [Full Text] [PDF]
|
|
|
|
|
|
A. Ilercil, R. B. Devereux, M. J. Roman, M. Paranicas, M. J. O'Grady, E. T. Lee, T. K. Welty, R. R. Fabsitz, and B. V. Howard Associations of Insulin Levels With Left Ventricular Structure and Function in American Indians : The Strong Heart Study Diabetes, May 1, 2002; 51(5): 1543 - 1547. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. R. Williams Racial/Ethnic Variations in Women's Health: The Social Embeddedness of Health Am J Public Health, April 1, 2002; 92(4): 588 - 597. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. J. Rith-Najarian, D. M. Gohdes, R. Shields, B. Skipper, K. R. Moore, B. Tolbert, T. Raymer, and K. J. Acton Regional Variation in Cardiovascular Disease Risk Factors Among American Indians and Alaska Natives With Diabetes Diabetes Care, February 1, 2002; 25(2): 279 - 283. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Pedrinelli, G. Dell'Omo, G. Penno, and M. Mariani Non-diabetic microalbuminuria, endothelial dysfunction and cardiovascular disease Vascular Medicine, November 1, 2001; 6(4): 257 - 264. [Abstract] [PDF]
|
|
|
|
|
|
V. Palmieri, A. Celentano, M. J. Roman, G. de Simone, M. R. Lewis, L. Best, E. T. Lee, D. C. Robbins, B. V. Howard, and R. B. Devereux Fibrinogen and Preclinical Echocardiographic Target Organ Damage: The Strong Heart Study Hypertension, November 1, 2001; 38(5): 1068 - 1074. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. J. Acton, R. Shields, S. Rith-Najarian, B. Tolbert, J. Kelly, K. Moore, L. Valdez, B. Skipper, and D. Gohdes Applying the Diabetes Quality Improvement Project Indicators in the Indian Health Service Primary Care Setting Diabetes Care, January 1, 2001; 24(1): 22 - 26. [Abstract] [Full Text]
|
|
|
|
|
|
P. M. Okin, R. B. Devereux, B. V. Howard, R. R. Fabsitz, E. T. Lee, and T. K. Welty Assessment of QT Interval and QT Dispersion for Prediction of All-Cause and Cardiovascular Mortality in American Indians : The Strong Heart Study Circulation, January 4, 2000; 101(1): 61 - 66. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. L. Sievers, P. H. Bennett, J. Roumain, and R. G. Nelson Effect of Hypertension on Mortality in Pima Indians Circulation, July 6, 1999; 100(1): 33 - 40. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. M. Okin, R. B. Devereux, R. R. Fabsitz, E. T. Lee, J. M. Galloway, and B. V. Howard Principal Component Analysis of the T Wave and Prediction of Cardiovascular Mortality in American Indians: The Strong Heart Study Circulation, February 12, 2002; 105(6): 714 - 719. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. N. Bella, V. Palmieri, M. J. Roman, J. E. Liu, T. K. Welty, E. T. Lee, R. R. Fabsitz, B. V. Howard, and R. B. Devereux Mitral Ratio of Peak Early to Late Diastolic Filling Velocity as a Predictor of Mortality in Middle-Aged and Elderly Adults: The Strong Heart Study Circulation, April 23, 2002; 105(16): 1928 - 1933. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||