Published online before print March 24, 2003, doi: 10.1161/01.HYP.0000064181.63546.53
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
(Hypertension. 2003;41:1086.)
© 2003 American Heart Association, Inc.
Scientific Contributions |
Racial Differences in the Prevalence of Hypertensive Retinopathy
From the Singapore National Eye Center and National University of Singapore (T.Y.W.), Singapore; Department of Ophthalmology, University of Wisconsin (R.K., B.E.K.K., L.D.H.), Madison; Social Medicine Department, School of Medicine, Federal University of Rio Grande do Sul (B.B.D.), Porto Alegre, RS Brazil; Department of Population Health Sciences, University of Wisconsin (F.J.N.), Madison; Department of Biostatistics, University of North Carolina (D.J.C.), Chapel Hill; Department of Epidemiology, Johns Hopkins University (A.R.S.), Baltimore, Md.
Correspondence to Tien Yin Wong, MD, PhD, Department of Ophthalmology, National University of Singapore, 10 Kent Ridge Crescent, Singapore 119260, SINGAPORE. E-mail ophwty{at}nus.edu.sg
 |
Abstract |
|---|
 Top Abstract IntroductionMethodsResultsDiscussionReferences |
|---|
Few population-based data support the hypothesis that hypertensive retinopathy is more common in African Americans than in whites. We examined racial differences in the prevalence of and risk factors for hypertensive retinopathy in a population-based sample of 1860 African Americans and 7874 white persons, aged 49 to 73 years, without diabetes. Retinal photographs were taken of one randomly selected eye and evaluated for the presence of retinopathy (flame and blot-shaped retinal hemorrhages, microaneurysms, and soft exudates) according to standardized protocols by graders masked to participant characteristics. The prevalence of retinopathy was 2 times higher in African Americans than in whites (7.7% versus 4.1%, age- and gender-adjusted odds ratio [OR] 2.03, 95% confidence intervals [CI] 1.65, 2.49). After controlling for 6-year mean arterial blood pressure, use of antihypertensive medications and left ventricular hypertrophy by ECG criteria, the excess prevalence of retinopathy in African Americans was reduced by 40% (adjusted OR 1.61, 95% CI 1.26, 2.06). Further adjustment for other vascular risk factors, common carotid artery intima-media thickness, and serum creatinine levels reduced the excess prevalence in African Americans by another 13% (adjusted OR 1.48, 95% CI 1.08, 2.03). We conclude that hypertensive retinopathy is twice as frequent in African Americans compared with whites without diabetes and that the excess prevalence of retinopathy in African Americans is associated with blood pressure and severity of hypertension.
Key Words: hypertension, genetic • blacks • race • microcirculation • retinopathy • blood pressure
|
Introduction |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
The higher prevalence of hypertension in African Americans compared with white persons in the United States is well documented.1–3 Studies show that African Americans are more likely to develop hypertensive-related complications (eg, left ventricular hypertrophy,4,5 hypertensive kidney disease,6–8 and stroke9), to have higher mortality rates,10 and to have poorer access to antihypertensive treatment.3
An important clinical marker of hypertensive end-organ damage is the presence of retinopathy, a spectrum of lesions seen in the retina resulting from hypertensive injury to the microvasculature (eg, retinal hemorrhages, microaneurysms).11,12 Black people of African descent have long been suggested to have an excess risk of hypertensive retinopathy.13–16 However, the few existing studies available that suggest possible racial differences have important limitations. First, most studies were based on highly selected clinic samples not representative of the general population.13,14 Second, the majority has relied on the use of clinical ophthalmoscopy to detect retinopathy,13–15 an unreliable method.17 Finally, older studies were conducted before the widespread use of antihypertensive treatment.13–16 Thus, whether hypertensive retinopathy is more common in African Americans in contemporary United States communities, and whether this is related to racial difference in blood pressure or other factors remains uncertain.
In the current study, we describe the prevalence of hypertensive retinopathy in community-based samples of African American and white persons living in the United States and examine risk factors that may account for possible racial differences in the prevalence of retinopathy.
|
Methods |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Study Population
The Atherosclerosis Risk In Communities (ARIC) study is a population-based study that included 15 792 women and men 45 to 64 years of age at recruitment in 1987–1989.18 Population samples were selected from four US communities: Forsyth County, North Carolina; Jackson, Mississippi (blacks only); and suburbs of Minneapolis, Minnesota; and Washington County, Maryland. More than 90% of the African American participants were from Jackson. Of those examined at baseline, 14 346 (93% of survivors) returned for a second examination approximately 3 years later (1990–1992) and 12 887 (86% of the survivors) returned for a third examination approximately 6 years later (1993–1995).
Retinal photographs were taken at the third examination when the participants were 51 to 72 years of age.19 Of 12 887 participants who returned for this examination, we excluded 38 whose race was neither African American nor white, 42 nonwhite residents in Minneapolis and Maryland, and 1012 with no photographs, ungradable photographs, or retinal vascular occlusions. Because diabetes may complicate the definition of hypertensive retinopathy, we also excluded 1674 persons with diabetes (defined as a fasting glucose 
7.0 mmol/L, a nonfasting glucose 11.1 mmol/L, or a self-reported history of treatment for diabetes at any examination), and 387 with missing blood pressure or diabetes data at any examination. These exclusions left 9734 persons available for this analysis.
Institutional review boards at each study site and the Retinal Reading Center approved the study. Informed consent was obtained from all participants.
Definition of Retinopathy
The retinal photography procedure and its assessment have been reported.19 Briefly, after 5 minutes of dark adaptation, a 45-degree retinal photograph was taken of one randomly selected eye, centered on the optic disc and macula. Trained graders who were masked to participant identity evaluated the retinal photographs, according to a standardized protocol, for the presence or absence of retinal changes.19 In each quadrant, the following retinopathy lesions were graded: flame-shaped hemorrhages, blot and dot hemorrhages, microaneurysms, cotton wool spots (soft exudates), and disk swelling. Each lesion was classified as definite, probable, or none in each quadrant. Retinopathy was defined as "present" if any of these lesions were definite or probable in any of the 4 quadrants.20 Reliability of the grading has been previously reported.21 In general, intra- and inter-grader kappa statistics of specific retinal lesions ranged from 0.76 to 1.00, respectively.21
Definition of Risk Factors
Participants underwent a standardized interview, clinical examination, and laboratory investigations in the ARIC study.22 At each visit, blood pressures were taken with a random-zero sphygmomanometer, and the mean of the last 2 measurements was used for analyses. Hypertension was defined as systolic blood pressure 140 mm Hg, diastolic blood pressure 90 mm Hg, or use of antihypertensive medication during the previous 2 weeks. Mean arterial blood pressure was also computed as 2/3 of the diastolic plus 1/3 of the systolic value. Current blood pressure was defined as measurements at the time of retinal photography (third ARIC examination), whereas 3- and 6-year past blood pressures were defined as measurements taken 3 and 6 years before retinal photography (first and second ARIC examinations). The 6-year mean arterial blood pressure (average of the 3 examinations) was used as a covariate to adjust for the effects of blood pressure.20 Left ventricular hypertrophy was defined from electrocardiographic criteria, described previously.22
Blood collection and processing followed a standard protocol.22 Total plasma cholesterol was measured by enzymatic methods, HDL cholesterol was measured after dextran-magnesium precipitation of the non-HDL lipoproteins, and glucose was assessed by a modified hexokinase/glucose-6-phosphate dehydrogenase procedure.22 Serum creatinine level was measured using a modified kinetic Jaffe method.22 Technicians measured height and weight with participants in scrub suits, and body mass index (BMI) was calculated as weight/height2 (kg/m2). Physical activity, education, occupation, cigarette smoking, and alcohol consumption were ascertained from interview. Physical activity was characterized by a sports index, with values ranging from 1 to 5.23 Coronary heart disease (CHD) at baseline was defined on the basis of a medical history, and incident CHD events were defined using symptoms, ECG, and biomarker levels.22 The cumulative prevalence (prevalence CHD and incident CHD up to the third ARIC examination) was used to define absence versus presence of CHD. Measurement of common carotid artery intima-media thickness (IMT) by ultrasound followed a standard protocol.22 All variables were based on data from the third examination, except for IMT and left ventricular hypertrophy (first examination), serum creatinine (second examination), and 6-year mean arterial blood pressure (average of 3 examinations).
Statistical Methods
We compared participant characteristics and the prevalence of retinopathy in African Americans and whites using analysis of covariance models or logistic regression models to adjust for age and gender. We used logistic regression models to calculate odds ratios (OR) for retinopathy associated with race (African Americans versus whites) and specific risk factors (eg, presence versus absence of hypertension or a 10 mm Hg difference in current or past mean arterial blood pressure), adjusting for age and gender.
To evaluate the extent that blood pressure and other risk factors might explain the excess prevalence of retinopathy in African Americans compared with whites, we estimated the percentage reduction in odds associated with adjustment for these factors according to the following formula: (ra-rb)/(ra-1)x100, where ra is the OR of retinopathy in African Americans compared with whites, adjusted for age and gender only (reference Model 1), and rb is the OR after additional adjustment in Models 2 to 4. These were grouped as follows: Model 2: age-, gender-, and hypertension-related factors (6-year mean arterial blood pressure, antihypertensive medications use, and left ventricular hypertrophy); Model 3: variables in Model 2 plus other cardiovascular risk factors (total and HDL cholesterol, fasting glucose, BMI, sports index, smoking and alcohol consumption status, education, occupation); and Model 4: variables in Model 3 plus indices of subclinical macrovascular and renal microvascular disease (common carotid IMT and serum creatinine).
|
Results |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Table 1 shows participant characteristics of African Americans and whites. African Americans were slightly younger than whites and less likely to be men. After adjusting for age and gender, African Americans were more likely to have hypertension, higher blood pressure, left ventricular hypertrophy, lower education levels, higher HDL cholesterol, higher BMI, and higher serum creatinine, and they were less likely to have ever smoked cigarettes or drunk alcohol. Smaller differences were seen for fasting glucose levels (slightly higher in African Americans), age, total plasma cholesterol, and physical activity (slightly higher in whites).
|
The prevalence of retinopathy in African Americans and whites is shown in Table 2. African Americans were more likely to have retinopathy than whites (7.7% vs 4.1%). This pattern was seen in persons with (9.1% vs 5.3%) and without (5.9% vs 3.6%) hypertension.
|
Associations of retinopathy with race and other risk factors are shown in Table 3. After adjusting for age and gender, retinopathy was significantly associated with African American race, hypertension status, current and past blood pressure, presence of left ventricular hypertrophy, lower education levels, higher fasting glucose, higher BMI, lower sports activity index, abstention from alcohol, and greater common carotid artery IMT. When the results were stratified by race, most of the associations were no longer significant. Retinopathy was associated with hypertension status in both African Americans and whites, but associations with current and past blood pressure was stronger and significant only in African Americans. Higher fasting glucose was significantly associated with retinopathy in whites only.
|
We evaluated factors that may explain the higher prevalence of retinopathy among African Americans (Table 4). We estimated the reduction in odds of retinopathy associated with African American race with adjustment of specific factors (Models 2 to 4). The OR of retinopathy associated with African American race (age- and gender-adjusted OR of 2.03, Model 1) was reduced by 40% after controlling for 6-year mean arterial blood pressure, use of antihypertensive medications, and left ventricular hypertrophy (adjusted OR of 1.61, Model 2). Further adjustment for other vascular risk factors, common carotid artery IMT, and serum creatinine levels reduced the excess prevalence of retinopathy in African Americans marginally (Models 3 and 4). In people with hypertension, the OR of retinopathy associated with African American race (age- and gender-adjusted OR of 1.89, Model 1) was reduced by 45% after adjustment for 6-year mean arterial blood pressure, antihypertensive medication use, and left ventricular hypertrophy (adjusted OR of 1.49, Model 2), which was reduced by a further 25% with additional adjustment for other factors (adjusted OR of 1.26, Model 4). In contrast, in persons without hypertension, the OR of retinopathy associated with African American race (age- and gender-adjusted OR of 1.77, Model 1) was not altered substantially in models controlling for blood pressure and other factors (Models 2 to 4). Results were essentially similar in analyses adjusting for systolic or diastolic blood pressure (data not shown).
|
Because most of the African Americans were from Jackson and only one site (Forsyth County) had both racial groups, we repeated the analysis limited to Forsyth County participants only (n=2445 whites and n=214 African Americans). The prevalence of retinopathy was 2 times higher in African Americans (9.3%) than in whites (4.3%) living in Forsyth County.
Finally, we conducted subsidiary analyses for specific retinopathy lesions (ie, retinal hemorrhages, microaneurysms, and soft exudates), in men and women separately, including people with diabetes (n=1674). The results were not qualitatively different (data not shown).
|
Discussion |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Hypertensive retinopathy reflects microvascular damage resulting mainly from elevated blood pressure, is a marker of subclinical cerebral disease,24 and is associated with risk of stroke20,24 and higher mortality in people with hypertension.25,26 Thus, both the Joint National Committee on the Prevention, Detection, Evaluation, and Treatment of High Blood Pressure27 and the British Society of Hypertension28 have recommended that retinopathy is an indication for initiating antihypertensive drug therapy, even in persons with mild hypertension (systolic/diastolic blood pressures of 140 to 159/90 to 99 mm Hg).
In the current study, we showed that hypertensive retinopathy, as assessed from retinal photographs, is twice as frequent in African Americans as in whites living in the United States, with the excess prevalence occurring in people with and without hypertension. We further showed that the higher prevalence of retinopathy in African Americans is substantially diminished after controlling for 6-year average arterial blood pressure and severity of hypertension (as indexed by use of antihypertensive medications and left ventricular hypertrophy). Additional adjustment for other cardiovascular risk factors, common carotid artery disease, and serum creatinine reduced the racial difference in retinopathy prevalence only marginally.
Our findings provide the first documentation of higher prevalence of hypertensive retinopathy in African Americans in contemporary, community-based populations in the United States. This is consistent with previous smaller studies in the literature, mostly conducted in the 1960s and 1970s, that show black people of African descent have a higher prevalence of hypertensive retinopathy than white people of European ethnicity.13–16 In a study in England, the prevalence of hypertensive retinal changes, as defined from retinal photographs, was higher in the 299 participants of Afro-Caribbean origin than in the 384 participants of European origin.16 The study noted that differences in resting blood pressure between Afro-Caribbean and Europeans could not fully account for the racial difference in retinopathy prevalence, although no data on other possible cardiovascular risk factors that may explain the excess prevalence of retinopathy in Afro-Caribbean people were available.
There are several possible explanations for the excess prevalence of retinopathy in African Americans. First, differences in the blood pressure and severity of hypertension (as reflected by the use of antihypertensive medications and the presence of left ventricular hypertrophy) explained almost half of the excess prevalence of retinopathy in African Americans. Racial differences in other vascular risk factors, socioeconomic status, and subclinical macrovascular (as reflected by common carotid artery IMT) and microvascular (serum creatinine) disease explained some of the remaining racial difference in retinopathy. It is likely that we were unable to adequately control for racial differences in the cumulative exposure to elevated blood pressure or other risk factors, so that residual confounding from these may still contribute to the racial differences observed. Second, the retinopathy lesions may reflect pathogenic processes involving the endothelium and microvasculature not measured here. Thus, differences in the frequency of these conditions or processes may contribute to the racial difference in retinopathy prevalence. The fact that blood pressure and standard vascular risk factors did not explain the racial difference in retinopathy prevalence in the subgroup of people without a history of hypertension lends supports to this latter hypothesis (Table 4). Third, poorly understood differences in the susceptibility to retinal vascular damage from elevated blood pressure may contribute to the higher prevalence of retinopathy in African Americans.3,29,30
We note that "normotensive" participants also had retinal signs traditionally classified as "hypertensive retinopathy" (Table 2). This is partly related to measurement error in our definition of hypertension (ie, single blood pressure measurements only partially reflect a person’s lifetime history of "exposure" to hypertension) and partly to the fact that some retinal signs are related to aging (eg, arteriosclerosis) and other nonhypertensive processes (eg, ocular ischemia from carotid artery disease).11,12
Our study may have important public health and clinical implications. The higher prevalence of retinopathy in middle-aged African Americans with hypertension is disturbing (9.1%) because retinopathy is associated with an increased risk of cerebrovascular disease and mortality.12,20,24 These findings reemphasize the importance of current public health approaches to tackling hypertension in this racial group. Additionally, the higher prevalence of retinopathy in African Americans supports the growing literature that this racial group is more likely to have cerebral microvascular disease such as lacunar stroke31 and white matter lesions (which are thought to be microvascular in nature),24 but less likely to have extracranial macrovascular disease such as carotid artery atherosclerosis.32,33
The strengths of the current study include its population-based nature, the quantitative and masked evaluation of retinopathy, standardized assessment of blood pressure, and data on other risk factors. Study limitations should be highlighted. First, because retinal photographs were taken 6 years into the ARIC study, selection biases may have attenuated or accentuated some findings. If African Americans with retinopathy were more likely to die before photography, these associations could be attenuated. Second, the ARIC study did not employ pharmacological pupillary dilation before photography, and therefore, a high percentage of photographs was ungradable. We have previously found that African Americans were more likely to have ungradable retinal photographs than whites.19 In addition, only one eye was photographed. Although hypertensive retinopathy is often symmetrical between eyes, it is possible that some retinopathy was missed because of the possibility of the involved eye not being photographed. However, we have no reason to believe these factors would lead to a differential detection of retinopathy between African Americans and whites. Fourth, we cannot exclude the possibility that geographical differences contribute to the disparity in retinal prevalence. Nonetheless, the results were not substantially different in analyses restricted to one site with both African Americans and whites (Forsyth County). Finally, because diabetes complicates the assessment of hypertensive retinopathy, we excluded persons with diabetes from these analyses. In a subsidiary analysis with diabetics included, we found a higher OR of hypertensive retinopathy associated with African American race (age- and gender-adjusted OR of 2.44 compared with an OR of 2.03, as shown in Table 4). Thus, we may have underestimated the racial differences in hypertensive retinopathy.
Perspective
Hypertensive retinopathy is twice as common in middle-aged African Americans as in whites. Racial difference in the prevalence of retinopathy is closely linked to racial differences in blood pressure levels and hypertension severity, suggesting that appropriate strategies to control hypertension in African Americans may reduce this disparity.
|
Acknowledgments |
|---|
This study was supported by contracts N01-HC-35125, N01-HC-35126, N01-HC-55015, N01-HC-55016, N01-HC-55018, N01-HC-55019, N01-HC-55020, N01-HC-55021, and N01-HC-55022 from the National Heart, Lung, and Blood Institute, Bethesda, Md. The authors thank the staff and participants in the ARIC study for their important contributions.
Received December 18, 2002; first decision January 26, 2003; accepted February 14, 2003.
|
References |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
- Cornoni-Huntley J, LaCroix AZ, Havlik RJ. Race and sex differentials in the impact of hypertension in the United States. The National Health and Nutrition Examination Survey I Epidemiologic Follow-Up Study. Arch Intern Med. 1989; 149: 780–788.[Abstract]
- Klag MJ, Whelton PK, Coresh J, Grim CE, Kuller LH. The association of skin color with blood pressure in US blacks with low socioeconomic status. JAMA. 1991; 265: 599–602.[Abstract]
- Gillum RF. Pathophysiology of hypertension in blacks and whites. A review of the basis of racial blood pressure differences. Hypertension. 1979; 1: 468–475.
[Abstract/Free Full Text] - Arnett DK, Rautaharju P, Crow R, Folsom AR, Ekelund LG, Hutchinson R, Tyroler HA, Heiss G. Black-white differences in electrocardiographic left ventricular mass and its association with blood pressure (the ARIC study). Atherosclerosis Risk in Communities. Am J Cardiol. 1994; 74: 247–252.[CrossRef][Medline] [Order article via Infotrieve]
- Alexander M, Grumbach K, Selby J, Brown AF, Washington E. Hospitalization for congestive heart failure. Explaining racial differences. JAMA. 1995; 274: 1037–1042.[Abstract]
- Perneger TV, Klag MJ, Feldman HI, Whelton PK. Projections of hypertension-related renal disease in middle-aged residents of the United States. JAMA. 1993; 269: 1272–1277.[Abstract]
- Klag MJ, Whelton PK, Randall BL, Neaton JD, Brancati FL, Stamler J. End-stage renal disease in African American and white men. 16-year MRFIT findings. JAMA. 1997; 277: 1293–1298.[Abstract]
- McClellan W, Tuttle E, Issa A. Racial differences in the incidence of hypertensive end-stage renal disease (ESRD) are not entirely explained by differences in the prevalence of hypertension. Am J Kidney Dis. 1988; 12: 285–290.[Medline] [Order article via Infotrieve]
- Kittner SJ, White LR, Losonczy KG, Wolf PA, Hebel JR. Black-white differences in stroke incidence in a national sample. The contribution of hypertension and diabetes mellitus. JAMA. 1990; 264: 1267–1270.[Abstract]
- Otten MW Jr, Teutsch SM, Williamson DF, Marks JS. The effect of known risk factors on the excess mortality of black adults in the United States. JAMA. 1990; 263: 845–850.[Abstract]
- Tso MOM, Jampol LM. Pathophysiology of hypertensive retinopathy. Ophthalmology. 1982; 89: 1132–1145.[Medline] [Order article via Infotrieve]
- Wong TY, Klein R, Klein BEK, Tielsch JM, Hubbard LD, Nieto FJ. Retinal microvascular abnormalities and their relations with hypertension, cardiovascular diseases and mortality. Surv Ophthalmol. 2001; 46: 59–80.[CrossRef][Medline] [Order article via Infotrieve]
- Schneckloth RE, Stuart KL, Moore FE. Arterial pressure and hypertensive disease in a West Indian Negro population: report of a survey in St Kitts, West Indies. Am Heart J. 1962; 63: 607–628.[CrossRef][Medline] [Order article via Infotrieve]
- Ladipo GOA. Hypertensive retinopathy in Nigerians: a prospective clinical study of 350 cases. Trop Geogr Med. 1981; 33: 311–316.[Medline] [Order article via Infotrieve]
- McDonough JR, Garrison GE, Hames CG. Blood pressure and hypertensive disease among Negroes and whites. Ann Intern Med. 1964; 61 (suppl 6): 208–228.[Medline] [Order article via Infotrieve]
- Sharp PS, Chaturvedi N, Wormald R, McKeigue PM, Marmot MG, Young SM. Hypertensive retinopathy in Afro-Caribbeans and Europeans. Prevalence and risk factor relationships. Hypertension. 1995; 25: 1322–1325.
[Abstract/Free Full Text] - Dimmitt SB, West JN, Eames SM, Gibson JM, Gosling P, Littler WA. Usefulness of ophthalmoscopy in mild to moderate hypertension. Lancet. 1989; 1: 1103–1106.[Medline] [Order article via Infotrieve]
- The ARIC Investigators. The Atherosclerosis Risk in Communities (ARIC) Study: design and objectives. Am J Epidemiol. 1989; 129: 687–702.
[Abstract/Free Full Text] - Hubbard LD, Brothers RJ, King WN, Clegg LX, Klein R, Cooper LS, Sharrett AR, Davis MD, Cai J. Methods for evaluation of retinal microvascular abnormalities associated with hypertension/sclerosis in the Atherosclerosis Risk in Communities Study. Ophthalmology. 1999; 106: 2269–2280.[CrossRef][Medline] [Order article via Infotrieve]
- Wong TY, Klein R, Couper DJ, Cooper LS, Shahar E, Hubbard LD, Wofford MR, Sharrett AR. Retinal microvascular abnormalities and incident strokes. The Atherosclerosis Risk in the Communities Study. Lancet. 2001; 358: 1134–1140.[CrossRef][Medline] [Order article via Infotrieve]
- Couper DJ, Klein R, Hubbard LD, Wong TY, Sorlie PD, Cooper LS, Brothers RJ, Nieto FJ. Reliability of retinal photography in the assessment of retinal microvascular characteristics: the Atherosclerosis Risk in the Communities Study. Am J Ophthalmology. 2002; 133: 78–88.[CrossRef][Medline] [Order article via Infotrieve]
- National Heart, Lung, and Blood Institute. Atherosclerosis Risk in Communities Study. Operations Manual No. 2, Cohort Component Procedures, Version 2.0. Chapel Hill, NC: ARIC Coordinating Center, School of Public Health, University of North Carolina; 1988.
- Baecke JA, Burema J, Frijters JE. A short questionnaire for the measurement of habitual physical activity in epidemiological studies. Am J Clin Nutr. 1982; 36: 936–942.
[Abstract/Free Full Text] - Wong TY, Klein R, Sharrett AR, Couper DJ, Klein BE, Liao DP, Hubbard LD, Mosley TH. Cerebral white matter lesion, retinopathy and risk of clinical stroke: the Atherosclerosis Risk in the Communities Study. JAMA. 2002; 288: 67–74.
[Abstract/Free Full Text] - Palmer RS, Loofbourow D, Doering CR. Prognosis in essential hypertension: eight-year follow-up study of 430 patients on conventional medical treatment. N Engl Med J. 1948; 239: 990.[Medline] [Order article via Infotrieve]
- Breslin DJ, Gifford RW Jr, Fairbairn JF II, Kearns TP. Prognostic importance of ophthalmoscopic findings in essential hypertension. JAMA. 1966; 195: 335–338.[CrossRef][Medline] [Order article via Infotrieve]
- Joint National Committee on the Prevention, Detection, Evaluation, and Treatment of High Blood Pressure. Sixth Report. Bethesda, Md: National Institutes of Health Publication 98–4080; 1997.
- Ramsay LE, Williams B, Johnston GD, MacGregor GA, Poston L, Potter JF, Poulter NR, Russell G. British Hypertension Society guidelines for hypertension management 1999: summary. BMJ. 1999; 319: 630–635.
[Free Full Text] - Murray RF Jr. Skin color and blood pressure. Genetics or environment? JAMA. 1991; 265: 639–640.[CrossRef][Medline] [Order article via Infotrieve]
- Devereux RB, Okin PM, Roman MJ. Pre-clinical cardiovascular disease and surrogate end-points in hypertension: does race influence target organ damage independent of blood pressure? Ethn Dis. 1998; 8: 138–148.[Medline] [Order article via Infotrieve]
- Caplan LR, Gorelick PB, Hier DB. Race, sex and occlusive cerebrovascular disease: a review. Stroke. 1986; 17: 648–655.
[Free Full Text] - Ryu JE, Murros K, Espeland MA, Rubens J, McKinney WM, Toole JF, Crouse JR. Extracranial carotid atherosclerosis in black and white patients with transient ischemic attacks. Stroke. 1989; 20: 1133–1137.
[Abstract/Free Full Text] - Howard G, Sharrett AR, Heiss G, Evans GW, Chambless LE, Riley WA, Burke GL. Carotid artery intimal-medial thickness distribution in general populations as evaluated by B-mode ultrasound. ARIC Investigators. Stroke. 1993; 24: 1297–1304.
[Abstract/Free Full Text]
This article has been cited by other articles:
 |
|
 |
|
  T. T. Nguyen, J. J. Wang, and T. Y. Wong Retinal Vascular Changes in Pre-Diabetes and Prehypertension: New findings and their research and clinical implications Diabetes Care, October 1, 2007; 30(10): 2708 - 2715. [Full Text] [PDF]
|
|
|
|
 |
|
 B.-J. H van den Born, C. A A Hulsman, J. B L Hoekstra, R. O Schlingemann, and G. A van Montfrans Value of routine funduscopy in patients with hypertension: systematic review BMJ, July 9, 2005; 331(7508): 73. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Y. Wong and P. Mitchell Hypertensive Retinopathy N. Engl. J. Med., November 25, 2004; 351(22): 2310 - 2317. [Full Text] [PDF]
|
|
|
|
 |
|
 J. J. Wang, P. Mitchell, H. Leung, E. Rochtchina, T. Y. Wong, and R. Klein Hypertensive Retinal Vessel Wall Signs in a General Older Population: The Blue Mountains Eye Study Hypertension, October 1, 2003; 42(4): 534 - 541. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||