Gender and racial differences in endothelial oxidative stress and inflammation in patients with symptomatic peripheral artery disease

Andrew W. Gardner, Donald E. Parker, Polly S. Montgomery, Danuta Sosnowska, Ana I. Casanegra, Zoltan Ungvari, Anna Csiszar, William E. Sonntag

Research output: Contribution to journalArticle

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Abstract

Background: We compared (1) cellular reactive oxygen species (ROS) production, inflammation, and apoptosis of cultured endothelial cells treated with sera and (2) circulating inflammatory measures, antioxidant capacity, vascular biomarkers, and calf muscle hemoglobin oxygen saturation (StO2) in men and women with peripheral artery disease (PAD). A secondary aim was to compare exercise performance and daily ambulatory activity between men and women. We hypothesized that women would have more impaired endothelial cellular ROS, inflammation, and apoptosis than men as well as worse systemic inflammation, antioxidant capacity, vascular biomarkers, calf muscle StO2, exercise performance, and daily ambulatory activity. Methods: The 148 symptomatic men and women with PAD were characterized on the endothelial effects of circulating factors present in the sera by a cell culture-based bioassay on primary human arterial endothelial cells. Patients were further evaluated by circulating inflammatory and vascular biomarkers, physical examination and medical history, exercise performance, and calf muscle StO2 during exercise, and ambulatory activity was monitored during 1 week. Results: Cellular ROS production was higher in African American women than in men (P =.021), but there was no gender difference in white individuals (P =.537). Men and women were not significantly different on endothelial cell apoptosis (P =.833) and nuclear factor κB activity (P =.465). For circulating factors, additional gender differences were found when comparisons were made within each race. In African Americans, women had higher intercellular adhesion molecule 1 (P =.022) and leptin (P <.001); whereas in white individuals, women had higher matrix metallopeptidase 9 (P =.047), higher vascular cell adhesion molecule 1 (P =.047), and lower hepatocyte growth factor (P =.046). Overall, women had higher apolipoprotein CIII (P =.035), lower pain-free distance (P =.048) and total distance (P <.001) during the 6-minute walk test, shorter time for calf muscle StO2 to reach the minimum value during exercise (P =.027), and slower average cadence (P =.004) during daily ambulation. Conclusions: African American women with symptomatic PAD have a heightened oxidative status, likely resulting in increased endothelial oxidative stress, compared with men. Furthermore, women exhibit a more pronounced proinflammatory profile of circulating biomarkers as well as more limited peripheral microcirculation, exercise performance, and ambulatory activity than men do. The clinical significance is that women with symptomatic PAD are in greater need than men of clinical intervention to improve oxidative stress, inflammation, and microcirculation, which may in turn have a favorable impact on their lower exercise performance and daily activity.

Original languageEnglish (US)
Pages (from-to)1249-1257
Number of pages9
JournalJournal of Vascular Surgery
Volume61
Issue number5
DOIs
StatePublished - May 1 2015

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Peripheral Arterial Disease
Oxidative Stress
Inflammation
Exercise
Biomarkers
African Americans
Blood Vessels
Reactive Oxygen Species
Muscles
Endothelial Cells
Microcirculation
Apoptosis
Antioxidants
Apolipoprotein C-III
Hepatocyte Growth Factor
Vascular Cell Adhesion Molecule-1
Metalloproteases
Intercellular Adhesion Molecule-1
Leptin
Serum

All Science Journal Classification (ASJC) codes

  • Surgery
  • Cardiology and Cardiovascular Medicine

Cite this

Gardner, Andrew W. ; Parker, Donald E. ; Montgomery, Polly S. ; Sosnowska, Danuta ; Casanegra, Ana I. ; Ungvari, Zoltan ; Csiszar, Anna ; Sonntag, William E. / Gender and racial differences in endothelial oxidative stress and inflammation in patients with symptomatic peripheral artery disease. In: Journal of Vascular Surgery. 2015 ; Vol. 61, No. 5. pp. 1249-1257.
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abstract = "Background: We compared (1) cellular reactive oxygen species (ROS) production, inflammation, and apoptosis of cultured endothelial cells treated with sera and (2) circulating inflammatory measures, antioxidant capacity, vascular biomarkers, and calf muscle hemoglobin oxygen saturation (StO2) in men and women with peripheral artery disease (PAD). A secondary aim was to compare exercise performance and daily ambulatory activity between men and women. We hypothesized that women would have more impaired endothelial cellular ROS, inflammation, and apoptosis than men as well as worse systemic inflammation, antioxidant capacity, vascular biomarkers, calf muscle StO2, exercise performance, and daily ambulatory activity. Methods: The 148 symptomatic men and women with PAD were characterized on the endothelial effects of circulating factors present in the sera by a cell culture-based bioassay on primary human arterial endothelial cells. Patients were further evaluated by circulating inflammatory and vascular biomarkers, physical examination and medical history, exercise performance, and calf muscle StO2 during exercise, and ambulatory activity was monitored during 1 week. Results: Cellular ROS production was higher in African American women than in men (P =.021), but there was no gender difference in white individuals (P =.537). Men and women were not significantly different on endothelial cell apoptosis (P =.833) and nuclear factor κB activity (P =.465). For circulating factors, additional gender differences were found when comparisons were made within each race. In African Americans, women had higher intercellular adhesion molecule 1 (P =.022) and leptin (P <.001); whereas in white individuals, women had higher matrix metallopeptidase 9 (P =.047), higher vascular cell adhesion molecule 1 (P =.047), and lower hepatocyte growth factor (P =.046). Overall, women had higher apolipoprotein CIII (P =.035), lower pain-free distance (P =.048) and total distance (P <.001) during the 6-minute walk test, shorter time for calf muscle StO2 to reach the minimum value during exercise (P =.027), and slower average cadence (P =.004) during daily ambulation. Conclusions: African American women with symptomatic PAD have a heightened oxidative status, likely resulting in increased endothelial oxidative stress, compared with men. Furthermore, women exhibit a more pronounced proinflammatory profile of circulating biomarkers as well as more limited peripheral microcirculation, exercise performance, and ambulatory activity than men do. The clinical significance is that women with symptomatic PAD are in greater need than men of clinical intervention to improve oxidative stress, inflammation, and microcirculation, which may in turn have a favorable impact on their lower exercise performance and daily activity.",
author = "Gardner, {Andrew W.} and Parker, {Donald E.} and Montgomery, {Polly S.} and Danuta Sosnowska and Casanegra, {Ana I.} and Zoltan Ungvari and Anna Csiszar and Sonntag, {William E.}",
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Gender and racial differences in endothelial oxidative stress and inflammation in patients with symptomatic peripheral artery disease. / Gardner, Andrew W.; Parker, Donald E.; Montgomery, Polly S.; Sosnowska, Danuta; Casanegra, Ana I.; Ungvari, Zoltan; Csiszar, Anna; Sonntag, William E.

In: Journal of Vascular Surgery, Vol. 61, No. 5, 01.05.2015, p. 1249-1257.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Gender and racial differences in endothelial oxidative stress and inflammation in patients with symptomatic peripheral artery disease

AU - Gardner, Andrew W.

AU - Parker, Donald E.

AU - Montgomery, Polly S.

AU - Sosnowska, Danuta

AU - Casanegra, Ana I.

AU - Ungvari, Zoltan

AU - Csiszar, Anna

AU - Sonntag, William E.

PY - 2015/5/1

Y1 - 2015/5/1

N2 - Background: We compared (1) cellular reactive oxygen species (ROS) production, inflammation, and apoptosis of cultured endothelial cells treated with sera and (2) circulating inflammatory measures, antioxidant capacity, vascular biomarkers, and calf muscle hemoglobin oxygen saturation (StO2) in men and women with peripheral artery disease (PAD). A secondary aim was to compare exercise performance and daily ambulatory activity between men and women. We hypothesized that women would have more impaired endothelial cellular ROS, inflammation, and apoptosis than men as well as worse systemic inflammation, antioxidant capacity, vascular biomarkers, calf muscle StO2, exercise performance, and daily ambulatory activity. Methods: The 148 symptomatic men and women with PAD were characterized on the endothelial effects of circulating factors present in the sera by a cell culture-based bioassay on primary human arterial endothelial cells. Patients were further evaluated by circulating inflammatory and vascular biomarkers, physical examination and medical history, exercise performance, and calf muscle StO2 during exercise, and ambulatory activity was monitored during 1 week. Results: Cellular ROS production was higher in African American women than in men (P =.021), but there was no gender difference in white individuals (P =.537). Men and women were not significantly different on endothelial cell apoptosis (P =.833) and nuclear factor κB activity (P =.465). For circulating factors, additional gender differences were found when comparisons were made within each race. In African Americans, women had higher intercellular adhesion molecule 1 (P =.022) and leptin (P <.001); whereas in white individuals, women had higher matrix metallopeptidase 9 (P =.047), higher vascular cell adhesion molecule 1 (P =.047), and lower hepatocyte growth factor (P =.046). Overall, women had higher apolipoprotein CIII (P =.035), lower pain-free distance (P =.048) and total distance (P <.001) during the 6-minute walk test, shorter time for calf muscle StO2 to reach the minimum value during exercise (P =.027), and slower average cadence (P =.004) during daily ambulation. Conclusions: African American women with symptomatic PAD have a heightened oxidative status, likely resulting in increased endothelial oxidative stress, compared with men. Furthermore, women exhibit a more pronounced proinflammatory profile of circulating biomarkers as well as more limited peripheral microcirculation, exercise performance, and ambulatory activity than men do. The clinical significance is that women with symptomatic PAD are in greater need than men of clinical intervention to improve oxidative stress, inflammation, and microcirculation, which may in turn have a favorable impact on their lower exercise performance and daily activity.

AB - Background: We compared (1) cellular reactive oxygen species (ROS) production, inflammation, and apoptosis of cultured endothelial cells treated with sera and (2) circulating inflammatory measures, antioxidant capacity, vascular biomarkers, and calf muscle hemoglobin oxygen saturation (StO2) in men and women with peripheral artery disease (PAD). A secondary aim was to compare exercise performance and daily ambulatory activity between men and women. We hypothesized that women would have more impaired endothelial cellular ROS, inflammation, and apoptosis than men as well as worse systemic inflammation, antioxidant capacity, vascular biomarkers, calf muscle StO2, exercise performance, and daily ambulatory activity. Methods: The 148 symptomatic men and women with PAD were characterized on the endothelial effects of circulating factors present in the sera by a cell culture-based bioassay on primary human arterial endothelial cells. Patients were further evaluated by circulating inflammatory and vascular biomarkers, physical examination and medical history, exercise performance, and calf muscle StO2 during exercise, and ambulatory activity was monitored during 1 week. Results: Cellular ROS production was higher in African American women than in men (P =.021), but there was no gender difference in white individuals (P =.537). Men and women were not significantly different on endothelial cell apoptosis (P =.833) and nuclear factor κB activity (P =.465). For circulating factors, additional gender differences were found when comparisons were made within each race. In African Americans, women had higher intercellular adhesion molecule 1 (P =.022) and leptin (P <.001); whereas in white individuals, women had higher matrix metallopeptidase 9 (P =.047), higher vascular cell adhesion molecule 1 (P =.047), and lower hepatocyte growth factor (P =.046). Overall, women had higher apolipoprotein CIII (P =.035), lower pain-free distance (P =.048) and total distance (P <.001) during the 6-minute walk test, shorter time for calf muscle StO2 to reach the minimum value during exercise (P =.027), and slower average cadence (P =.004) during daily ambulation. Conclusions: African American women with symptomatic PAD have a heightened oxidative status, likely resulting in increased endothelial oxidative stress, compared with men. Furthermore, women exhibit a more pronounced proinflammatory profile of circulating biomarkers as well as more limited peripheral microcirculation, exercise performance, and ambulatory activity than men do. The clinical significance is that women with symptomatic PAD are in greater need than men of clinical intervention to improve oxidative stress, inflammation, and microcirculation, which may in turn have a favorable impact on their lower exercise performance and daily activity.

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