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Epidemiology |

Complete Blood Cell Count and Retinal Vessel Diameters FREE

Barbara E. K. Klein, MD, MPH; Ronald Klein, MD, MPH; Chelsea E. Myers, MStat; Kristine E. Lee, MS
[+] Author Affiliations

Author Affiliations: Department of Ophthalmology and Visual Sciences, School of Medicine and Public Health, University of Wisconsin, Madison.


Section Editor: Leslie Hyman, PhD

More Author Information
Arch Ophthalmol. 2011;129(4):490-497. doi:10.1001/archophthalmol.2011.57.
Text Size: A A A
Published online

Objective  To examine the cross-sectional associations of components of the complete blood cell count with retinal vessel diameters.

Methods  The data are from the baseline examination of the Beaver Dam Eye Study cohort (n = 4730) from March 1, 1988, to September 14, 1990. Blood pressure was measured, a medical history including questions on cigarette smoking was obtained, and fundus photographs centered on the optic disc were taken and digitized. Retinal arteriole and venule diameters were measured using computer-assisted software. The central retinal arteriole equivalent and central retinal venule equivalent were computed. A complete blood cell count was done.

Results  In age- and sex-adjusted analyses, red blood cell count, hemoglobin level, hematocrit, and white blood cell count were all statistically significantly associated with central retinal venule equivalent and central retinal arteriole equivalent, while platelet count was associated only with central retinal venule equivalent. These relationships persisted in more fully adjusted models, except platelet count became statistically significantly associated with both central retinal arteriole equivalent and central retinal venule equivalent.

Conclusions  Blood components as measured in a complete blood cell count are significant correlates of retinal vessel diameters and should be considered in analyses where retinal blood vessel diameters are outcomes.

Retinal vessel diameters are associated with a variety of systemic traits and diseases. For example, narrower retinal arterioles are associated with higher blood pressure,14 myocardial perfusion,5 left ventricular remodeling,6 and stroke.7 Ikram et al8 have found that wider retinal arterioles are associated with impaired fasting glucose and diabetes. Wider retinal venules are associated with severity of diabetic retinopathy,9 and relatively smaller retinal venular diameters were found in persons with diabetes compared with those of similar age without type 2 diabetes9 and with incident proteinuria in persons with type 2 diabetes.10 Larger retinal venule diameters were associated with a variety of atherosclerosis indicators, such as higher carotid plaque scores and greater aortic calcifications, and risk factors such as body mass index and lower high-density lipoprotein cholesterol levels in the Rotterdam Study.11,12

It has been reported that hematocrit is significantly associated with retinal venular diameter,13 although in the few studies that have investigated this, relationships are not consistent.14 Also, white blood cell (WBC) count has been found to be associated with retinal venular diameters in a large population-based study.15 High WBC count, as is characteristic of leukemia,16 can alter the microvessel diameters owing to the high concentration of cells. Furthermore, it has been demonstrated in an experimental setting that leukocytosis in the peripheral and retinal circulation is associated with dilation of retinal arterioles and retinal venules.17 When retinal arterioles are embolized with glass microspheres in a laboratory setting, the diameters of the embolized vessels are clearly dilated to accommodate the particulate emboli.18

Because retinal vessels (arterioles and venules) are parts of dynamic microvascular beds that may reflect many physiological factors as well as the substances within them, we hypothesize that these structures may be influenced by the cells measured in the complete blood cell count in addition to other physiological factors. We examine this hypothesis in population-based data collected as part of the Beaver Dam Eye Study.

POPULATION

There were 4926 persons aged 43 to 86 years who participated in the baseline examination of the Beaver Dam Eye Study from March 1, 1988, to September 14, 1990. Ninety-nine percent of the population was of European ancestry.19 Informed consent was obtained from participants, and all examinations followed a similar protocol that was approved by the institutional human subjects committee of the University of Wisconsin and conformed to the tenets of the Declaration of Helsinki.

MEDICAL HISTORY

A medical history was obtained during the study evaluation. This included questions about cigarette smoking.

LABORATORY AND EXAMINATION METHODS

A complete blood cell count (Coulter counter method), a standardized medical history, measurements of blood pressure by standard protocol,20 and ocular examination with retinal photographs were obtained.20 Photographs of Early Treatment Diabetic Retinopathy Study field 1 were digitized and retinal vessel diameters were measured from these images with a computer-assisted standardized grading protocol.21,22

MEASUREMENT OF RETINAL VESSEL DIAMETERS

Stereoscopic 30° color retinal photographs were converted to digital images by a high-resolution scanner (Nikon LS2000; Nikon Corp, Tokyo, Japan) using standard settings for all photographs. Images were displayed on 21-in monitors set to 1600 × 1200 pixels. The diameters of all arterioles and venules coursing through a standard area 0.5 to 1.0 disc diameter from the optic disc margin (zone B) were measured using a customized computer program (Retinal Analysis; University of Wisconsin, Madison) according to a standard protocol. Each vessel was identified as an arteriole or venule by a trained grader, using the original color photograph for reference. The grader selected a segment of the vessel in zone B for measurement and used various tools to determine the validity of the measurement. A measurement was considered invalid if the grader could not get an accurate measurement after 3 attempts. The entire image was rejected if more than 1 arteriole or venule larger than 40 μm in diameter could not be measured accurately. This cutoff was based on preliminary data showing that vessels smaller than this diameter had no substantial effect on the summary values.21

DEFINITIONS

Cigarette smoking status was determined according to the following criteria: a never smoker had smoked fewer than 100 cigarettes in his or her lifetime; a past smoker had smoked 100 or more cigarettes in his or her lifetime but reported that he or she was no longer smoking; and a current smoker had smoked more than 100 cigarettes in his or her lifetime and reported that he or she was still smoking. Pack-years were calculated by first dividing the average number of cigarettes smoked per day by 20 and then multiplying by the number of years smoked.

STATISTICAL ANALYSIS

Statistical analyses were conducted in SAS version 9 statistical software (SAS Institute, Inc, Cary, North Carolina). Means were compared for statistically significant differences by the t test or analysis of variance when 2 or more than 2 groups, respectively, were involved. Because the distributions of the blood elements were highly skewed and differed by sex, each blood element was analyzed using sex-specific quintiles. We computed the quintiles for blood elements for each sex separately but analyzed the data with both sexes together (ie, quintile 1 [Q1] for men and Q1 for women were grouped together as Q1 for the entire group). Central retinal arteriolar equivalents (CRAEs) and central retinal venule equivalents (CRVEs) were computed based on the diameters of the 6 largest of each vessel type in standardized digitized photographs of the optic discs.21 Univariate analyses between each variable and CRAE and CRVE were conducted using simple linear regression. In additional analyses, age, sex, smoking status, diabetes status, and the other vessel measurement were added into a model sequentially to determine the effect on model fit. A final model for each blood element was developed using stepwise model selection.

Of the 4926 individuals who were interviewed and examined at the baseline examination, individuals were excluded from the analyses if there was no measurement for CRAE or CRVE in either eye (n = 114), if data were missing for any of the laboratory values used in the analysis (n = 14), or if the individual had a condition or disease such as leukemia, thrombocythemia, or polycythemia (n = 68). This left 4730 individuals eligible for analysis.

Excluded individuals were more likely to be older, female, and hypertensive and to have lower diastolic blood pressure and higher levels of glycated hemoglobin and all other blood elements except platelet count than those included. There were no differences in systolic blood pressure, pack-years smoked, platelet count, or current smoking between the 2 groups (Table 1).

Table Graphic Jump LocationTable 1. Characteristics of Persons Included and Excluded From Analysis

An increase of 1 sex-specific quintile of WBC count, red blood cell (RBC) count, hemoglobin level, and hematocrit was significantly associated with larger CRAE and CRVE (Table 2). An increase of 1 sex-specific quintile of platelet count was also significantly associated with larger CRVE. Additional adjustment for age did not change the significance of these relationships. When the elements were considered as continuous variables, the relationships were unchanged from when they were considered as quintiles.

Table Graphic Jump LocationTable 2. Relationships of Blood Elements With Central Retinal Arteriole Equivalent and Central Retinal Venule Equivalent

To investigate the relative strengths of the relationships of the blood elements to the vessel diameters, we developed models in which we sequentially included other known correlates of those diameters (Table 3). For all models, each element except platelet count was significantly associated with CRAE. The models indicate that including more of the additional variables increases the informativeness of the model measured by the change in R2. For all models, each blood element was significantly associated with CRVE. Additional adjustments for additional variables increased the R2 of the model. The presence of diabetes has a small incremental effect on the fit of the models.

Table Graphic Jump LocationTable 3. Multivariate Relationships Between Blood Elements and Central Retinal Arteriole and Venule Equivalentsa

We next performed the modeling using a stepwise approach including as possible variables all those considered in model 4 of Table 3 (Table 4 and Table 5). For CRAE, systolic blood pressure had the highest partial R2, followed by smoking status, blood element, and diabetes for each blood element. In the model assessing the contribution of platelet count to the other variables associated with CRAE, platelet count no longer contributed a significant amount of information. For CRVE, smoking status had the greatest partial R2, followed by the blood element and then sex and systolic blood pressure. Because of the importance of relative diameter, we repeated the analyses in Table 4, this time including CRVE in the models for CRAE and including CRAE in models for CRVE (Table 5). These additions markedly improved the R2 of all models. In all models, the relative importance of smoking status was diminished. The blood elements are the third most informative variable for CRVE or the fourth most informative variable for CRAE when controlling for the other vessel measurement.

Table Graphic Jump LocationTable 4. Stepwise Selection for Variables With Central Retinal Arteriole Equivalent and Central Retinal Venule Equivalent
Table Graphic Jump LocationTable 5. Stepwise Selection for Variables With Central Retinal Arteriole Equivalent and Central Retinal Venule Equivalent, With Central Retinal Venule Equivalent Considered for Central Retinal Arteriole Equivalent Models and Central Retinal Arteriole Equivalent Considered for Central Retinal Venule Equivalent Models

While the previous analyses considered each blood element individually, we next developed models in which they were included together. We chose only 1 of the 3 measures of RBC status (RBC count, hemoglobin level, and hematocrit) for the purposes of these analyses. We modeled the outcomes as was done in Table 4 and Table 5. In models where CRAE was the outcome and CRVE was not included, each of the blood element components added significantly to the models, with the RBC variables being most informative and WBC and platelet counts adding less information. When CRVE was included, the WBC count was no longer significant in the models. In models where CRVE was the outcome and CRAE was not included, each of the blood elements added significantly to the models; again, the RBC variables were the most informative and WBC and platelet counts added less information. When we added CRAE, all of the 3 blood components remained significant in most models. The relative importance of most of the other variables that were used in the models in Table 4 and Table 5 remained unchanged.

We have found that hematocrit, hemoglobin level, RBC count, WBC count, and platelet count are significantly associated with retinal vessel diameters. In addition, in our population these factors outweigh the relative importance of age, sex, and diabetes status in all models for both CRAE and CRVE. The effects related to RBC count are greater than those for WBC count. There are relatively smaller effects of platelet count. The associations are direct, ie, higher values are associated with wider diameters. While these data may indicate that these effects are related to that actual burden imposed by more particulate matter in the blood, it may be more informative to consider the physiological factors related to the blood elements (counts). It is possible that relative systemic factors such as chronic hypoxia due to systemic diseases or exposures may be associated with relatively higher RBC count (as well as hemoglobin level and hematocrit). An obvious exposure that is compatible with this notion is smoking, which we found to be associated with both CRAE and CRVE in analyses not adjusting for the diameter of either. Smoking, aside from potential effects on systemic hypoxia, is also associated with systemic inflammation. This mechanism has been invoked to explain previously described associations of WBC count to CRVE. In the Atherosclerosis Risk in Communities Study, higher WBC count was also associated with larger CRAE.13 Diabetes status, while significant in its effect, had a relatively small contribution compared with cigarette smoking for both CRAE and CRVE in our study.

Microvascular diameters undergo structural adaptation related to the local metabolic conditions.23 Hematocrit influences local hemodynamics.23 Vessel diameters are thought to change shear stress on vessel walls, dependent in part on oxygen deficit and RBC signaling.23 In the Rotterdam Study, retinal venule diameter was greater in persons with decreased cerebral blood flow and with decreased arteriolar oxygen saturation.11,24 Oxygen stimulation is associated with decreased flow-mediated diameters in large vessels.25 While this may have implications for cardiovascular events, it is uncertain what the health effect of changes in the microvascular beds may be.

Another possible effect (or correlate) of hematocrit is an increase in blood viscosity.26 This increase in viscosity has been shown to be associated with risk factors for cardiovascular disease such as blood lipid levels and blood pressure27 and may also be a pathway whereby the blood factors we examined influence retinal vessel diameters.

Our study is limited in that it is a cross-sectional analysis and these findings may not be applicable to longitudinal data. Also, while we have controlled for the most important confounders, there may be others that we did not measure or that were not important in our analyses but may be important in other studies. Lastly, variability of our outcome (as well as our covariate) measurements may have influenced our findings, although we suspect that these would have led to our underestimate of the relationships we report.

In summary, we have found that blood cell counts (and related measures of hematocrit and hemoglobin level) are significant correlates of retinal vessel diameters with greater effects than have been reported for some other correlates of these measures. We suggest that in research where retinal vessel diameters are the outcomes of interest, blood cell counts should be included as important determinants or correlates.

Correspondence: Barbara E. K. Klein, MD, MPH, Department of Ophthalmology and Visual Sciences, School of Medicine and Public Health, University of Wisconsin, Madison, 610 N Walnut St, Fourth Floor WARF, Madison, WI 53726-2336 (kleinb@epi.ophth.wisc.edu).

Submitted for Publication: May 13, 2010; final revision received August 26, 2010; accepted September 13, 2010.

Author Contributions: Dr B. E. K. Klein had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Financial Disclosure: None reported.

Funding/Support: This research is supported by grant EY06594 from the National Institutes of Health (Drs B. E. K. Klein and R. Klein). The National Eye Institute provided funding for the entire study, including collection and analyses of data. Additional support was provided by Senior Scientific Investigator Awards from Research to Prevent Blindness (Drs B. E. K. Klein and R. Klein).

Disclaimer: The content is solely the responsibility of the authors and does not necessarily reflect the official views of the National Eye Institute or the National Institutes of Health.

Additional Contributions: Heidi Gutt, BA, and Mary Kay Aprison, BS, assisted in editing and preparing the manuscript.

Gunn  M On ophthalmoscopic evidence of general arterial disease. Trans Ophthalmol Soc U K 1898;18356- 381
Friedenwald  H The Doyne Memorial Lecture: pathological changes in the retinal blood-vessels in arterio-sclerosis and hypertension. Trans Ophthalmol Soc U K 1930;50452- 531
Wagener  HPClay  GEGipner  JF Classification of retinal lesions in the presence of vascular hypertension: report submitted to the American Ophthalmological Society by the Committee on Classification of Hypertensive Disease of the Retina. Trans Am Ophthalmol Soc 1947;4557- 73
PubMed
Klein  RSharrett  ARKlein  BE  et al.  Are retinal arteriolar abnormalities related to atherosclerosis? the Atherosclerosis Risk in Communities Study. Arterioscler Thromb Vasc Biol 2000;20 (6) 1644- 1650
PubMed Link to Article
Wang  LWong  TYSharrett  ARKlein  RFolsom  ARJerosch-Herold  M Relationship between retinal arteriolar narrowing and myocardial perfusion: multi-ethnic study of atherosclerosis. Hypertension 2008;51 (1) 119- 126
PubMed Link to Article
Cheung  NBluemke  DAKlein  R  et al.  Retinal arteriolar narrowing and left ventricular remodeling: the multi-ethnic study of atherosclerosis. J Am Coll Cardiol 2007;50 (1) 48- 55
PubMed Link to Article
Wong  TYKlein  RCouper  DJ  et al.  Retinal microvascular abnormalities and incident stroke: the Atherosclerosis Risk in Communities Study. Lancet 2001;358 (9288) 1134- 1140
PubMed Link to Article
Ikram  MKJanssen  JARoos  AM  et al.  Retinal vessel diameters and risk of impaired fasting glucose or diabetes: the Rotterdam study. Diabetes 2006;55 (2) 506- 510
PubMed Link to Article
Klein  RKlein  BEMoss  SEWong  TYSharrett  AR Retinal vascular caliber in persons with type 2 diabetes: the Wisconsin Epidemiological Study of Diabetic Retinopathy: XX. Ophthalmology 2006;113 (9) 1488- 1498
PubMed Link to Article
Klein  RKlein  BEMoss  SEWong  TY Retinal vessel caliber and microvascular and macrovascular disease in type 2 diabetes, XXI: the Wisconsin Epidemiologic Study of Diabetic Retinopathy. Ophthalmology 2007;114 (10) 1884- 1892
PubMed Link to Article
Ikram  MKde Jong  FJVingerling  JR  et al.  Are retinal arteriolar or venular diameters associated with markers for cardiovascular disorders? the Rotterdam Study. Invest Ophthalmol Vis Sci 2004;45 (7) 2129- 2134
PubMed Link to Article
Ikram  MKWitteman  JCVingerling  JRBreteler  MMHofman  Ade Jong  PT Retinal vessel diameters and risk of hypertension: the Rotterdam Study. Hypertension 2006;47 (2) 189- 194
PubMed Link to Article
Klein  RKlein  BEKnudtson  MDWong  TYTsai  MY Are inflammatory factors related to retinal vessel caliber? the Beaver Dam Eye Study. Arch Ophthalmol 2006;124 (1) 87- 94
PubMed Link to Article
Kofoed  PKSander  BZubieta-Calleja  GKessel  LLarsen  M Retinal vessel diameters in relation to hematocrit variation during acclimatization of highlanders to sea level altitude. Invest Ophthalmol Vis Sci 2009;50 (8) 3960- 3963
PubMed Link to Article
Liew  GSharrett  ARKronmal  R  et al.  Measurement of retinal vascular caliber: issues and alternatives to using the arteriole to venule ratio. Invest Ophthalmol Vis Sci 2007;48 (1) 52- 57
PubMed Link to Article
Norén-Nyström  UHeyman  MFrisk  P  et al.  Vascular density in childhood acute lymphoblastic leukaemia correlates to biological factors and outcome. Br J Haematol 2009;146 (5) 521- 530
PubMed Link to Article
Kolodjaschna  JBerisha  FLasta  MPolska  EFuchsjäger-Mayrl  GSchmetterer  L Reactivity of retinal blood flow to 100% oxygen breathing after lipopolysaccharide administration in healthy subjects. Exp Eye Res 2008;87 (2) 131- 136
PubMed Link to Article
Klein  RKlein  BHenkind  PBellhorn  R Retinal collateral vessel formation. Invest Ophthalmol 1971;10 (7) 471- 480
PubMed
Klein  RKlein  BELinton  KLDe Mets  DL The Beaver Dam Eye Study: visual acuity. Ophthalmology 1991;98 (8) 1310- 1315
PubMed Link to Article
Hypertension Detection and Follow-up Program Cooperative Group, The hypertension detection and follow-up program. Prev Med 1976;5 (2) 207- 215
PubMed Link to Article
Knudtson  MDLee  KEHubbard  LDWong  TYKlein  RKlein  BE Revised formulas for summarizing retinal vessel diameters. Curr Eye Res 2003;27 (3) 143- 149
PubMed Link to Article
Wong  TYKlein  RSharrett  AR  et al.  The prevalence and risk factors of retinal microvascular abnormalities in older persons: the Cardiovascular Health Study. Ophthalmology 2003;110 (4) 658- 666
PubMed Link to Article
Reglin  BSecomb  TWPries  AR Structural adaptation of microvessel diameters in response to metabolic stimuli: where are the oxygen sensors? Am J Physiol Heart Circ Physiol 2009;297 (6) H2206- H2219
PubMed Link to Article
de Jong  FJVernooij  MWIkram  MK  et al.  Arteriolar oxygen saturation, cerebral blood flow, and retinal vessel diameters: the Rotterdam Study. Ophthalmology 2008;115 (5) 887- 892
PubMed Link to Article
Frøbert  OHolmager  PJensen  KMSchmidt  EBSimonsen  U Effect of acute changes in oxygen tension on flow-mediated dilation: relation to cardiovascular risk. Scand Cardiovasc J 2008;42 (1) 38- 47
PubMed Link to Article
Cinar  YDemir  GPaç  MCinar  AB Effect of hematocrit on blood pressure via hyperviscosity. Am J Hypertens 1999;12 (7) 739- 743
PubMed Link to Article
de Simone  GDevereux  RBChien  SAlderman  MHAtlas  SALaragh  JH Relation of blood viscosity to demographic and physiologic variables and to cardiovascular risk factors in apparently normal adults. Circulation 1990;81 (1) 107- 117
PubMed Link to Article

Figures

Tables

Table Graphic Jump LocationTable 1. Characteristics of Persons Included and Excluded From Analysis
Table Graphic Jump LocationTable 2. Relationships of Blood Elements With Central Retinal Arteriole Equivalent and Central Retinal Venule Equivalent
Table Graphic Jump LocationTable 3. Multivariate Relationships Between Blood Elements and Central Retinal Arteriole and Venule Equivalentsa
Table Graphic Jump LocationTable 4. Stepwise Selection for Variables With Central Retinal Arteriole Equivalent and Central Retinal Venule Equivalent
Table Graphic Jump LocationTable 5. Stepwise Selection for Variables With Central Retinal Arteriole Equivalent and Central Retinal Venule Equivalent, With Central Retinal Venule Equivalent Considered for Central Retinal Arteriole Equivalent Models and Central Retinal Arteriole Equivalent Considered for Central Retinal Venule Equivalent Models

References

Gunn  M On ophthalmoscopic evidence of general arterial disease. Trans Ophthalmol Soc U K 1898;18356- 381
Friedenwald  H The Doyne Memorial Lecture: pathological changes in the retinal blood-vessels in arterio-sclerosis and hypertension. Trans Ophthalmol Soc U K 1930;50452- 531
Wagener  HPClay  GEGipner  JF Classification of retinal lesions in the presence of vascular hypertension: report submitted to the American Ophthalmological Society by the Committee on Classification of Hypertensive Disease of the Retina. Trans Am Ophthalmol Soc 1947;4557- 73
PubMed
Klein  RSharrett  ARKlein  BE  et al.  Are retinal arteriolar abnormalities related to atherosclerosis? the Atherosclerosis Risk in Communities Study. Arterioscler Thromb Vasc Biol 2000;20 (6) 1644- 1650
PubMed Link to Article
Wang  LWong  TYSharrett  ARKlein  RFolsom  ARJerosch-Herold  M Relationship between retinal arteriolar narrowing and myocardial perfusion: multi-ethnic study of atherosclerosis. Hypertension 2008;51 (1) 119- 126
PubMed Link to Article
Cheung  NBluemke  DAKlein  R  et al.  Retinal arteriolar narrowing and left ventricular remodeling: the multi-ethnic study of atherosclerosis. J Am Coll Cardiol 2007;50 (1) 48- 55
PubMed Link to Article
Wong  TYKlein  RCouper  DJ  et al.  Retinal microvascular abnormalities and incident stroke: the Atherosclerosis Risk in Communities Study. Lancet 2001;358 (9288) 1134- 1140
PubMed Link to Article
Ikram  MKJanssen  JARoos  AM  et al.  Retinal vessel diameters and risk of impaired fasting glucose or diabetes: the Rotterdam study. Diabetes 2006;55 (2) 506- 510
PubMed Link to Article
Klein  RKlein  BEMoss  SEWong  TYSharrett  AR Retinal vascular caliber in persons with type 2 diabetes: the Wisconsin Epidemiological Study of Diabetic Retinopathy: XX. Ophthalmology 2006;113 (9) 1488- 1498
PubMed Link to Article
Klein  RKlein  BEMoss  SEWong  TY Retinal vessel caliber and microvascular and macrovascular disease in type 2 diabetes, XXI: the Wisconsin Epidemiologic Study of Diabetic Retinopathy. Ophthalmology 2007;114 (10) 1884- 1892
PubMed Link to Article
Ikram  MKde Jong  FJVingerling  JR  et al.  Are retinal arteriolar or venular diameters associated with markers for cardiovascular disorders? the Rotterdam Study. Invest Ophthalmol Vis Sci 2004;45 (7) 2129- 2134
PubMed Link to Article
Ikram  MKWitteman  JCVingerling  JRBreteler  MMHofman  Ade Jong  PT Retinal vessel diameters and risk of hypertension: the Rotterdam Study. Hypertension 2006;47 (2) 189- 194
PubMed Link to Article
Klein  RKlein  BEKnudtson  MDWong  TYTsai  MY Are inflammatory factors related to retinal vessel caliber? the Beaver Dam Eye Study. Arch Ophthalmol 2006;124 (1) 87- 94
PubMed Link to Article
Kofoed  PKSander  BZubieta-Calleja  GKessel  LLarsen  M Retinal vessel diameters in relation to hematocrit variation during acclimatization of highlanders to sea level altitude. Invest Ophthalmol Vis Sci 2009;50 (8) 3960- 3963
PubMed Link to Article
Liew  GSharrett  ARKronmal  R  et al.  Measurement of retinal vascular caliber: issues and alternatives to using the arteriole to venule ratio. Invest Ophthalmol Vis Sci 2007;48 (1) 52- 57
PubMed Link to Article
Norén-Nyström  UHeyman  MFrisk  P  et al.  Vascular density in childhood acute lymphoblastic leukaemia correlates to biological factors and outcome. Br J Haematol 2009;146 (5) 521- 530
PubMed Link to Article
Kolodjaschna  JBerisha  FLasta  MPolska  EFuchsjäger-Mayrl  GSchmetterer  L Reactivity of retinal blood flow to 100% oxygen breathing after lipopolysaccharide administration in healthy subjects. Exp Eye Res 2008;87 (2) 131- 136
PubMed Link to Article
Klein  RKlein  BHenkind  PBellhorn  R Retinal collateral vessel formation. Invest Ophthalmol 1971;10 (7) 471- 480
PubMed
Klein  RKlein  BELinton  KLDe Mets  DL The Beaver Dam Eye Study: visual acuity. Ophthalmology 1991;98 (8) 1310- 1315
PubMed Link to Article
Hypertension Detection and Follow-up Program Cooperative Group, The hypertension detection and follow-up program. Prev Med 1976;5 (2) 207- 215
PubMed Link to Article
Knudtson  MDLee  KEHubbard  LDWong  TYKlein  RKlein  BE Revised formulas for summarizing retinal vessel diameters. Curr Eye Res 2003;27 (3) 143- 149
PubMed Link to Article
Wong  TYKlein  RSharrett  AR  et al.  The prevalence and risk factors of retinal microvascular abnormalities in older persons: the Cardiovascular Health Study. Ophthalmology 2003;110 (4) 658- 666
PubMed Link to Article
Reglin  BSecomb  TWPries  AR Structural adaptation of microvessel diameters in response to metabolic stimuli: where are the oxygen sensors? Am J Physiol Heart Circ Physiol 2009;297 (6) H2206- H2219
PubMed Link to Article
de Jong  FJVernooij  MWIkram  MK  et al.  Arteriolar oxygen saturation, cerebral blood flow, and retinal vessel diameters: the Rotterdam Study. Ophthalmology 2008;115 (5) 887- 892
PubMed Link to Article
Frøbert  OHolmager  PJensen  KMSchmidt  EBSimonsen  U Effect of acute changes in oxygen tension on flow-mediated dilation: relation to cardiovascular risk. Scand Cardiovasc J 2008;42 (1) 38- 47
PubMed Link to Article
Cinar  YDemir  GPaç  MCinar  AB Effect of hematocrit on blood pressure via hyperviscosity. Am J Hypertens 1999;12 (7) 739- 743
PubMed Link to Article
de Simone  GDevereux  RBChien  SAlderman  MHAtlas  SALaragh  JH Relation of blood viscosity to demographic and physiologic variables and to cardiovascular risk factors in apparently normal adults. Circulation 1990;81 (1) 107- 117
PubMed Link to Article

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