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The Influence of Exercise on Cardiovascular Health in Sedentary Adults With Human Immunodeficiency Virus

Webel, Allison R. PhD, RN; Perazzo, Joseph PhD, RN; Longenecker, Christopher T. MD; Jenkins, Trevor MD; Sattar, Abdus PhD; Rodriguez, Margaret; Schreiner, Nate PhD, RN; Josephson, Richard A. MD, MS

Journal of Cardiovascular Nursing: May/June 2018 - Volume 33 - Issue 3 - p 239–247
doi: 10.1097/JCN.0000000000000450
ARTICLES: Exercise, Cardiovascular Health and HIV
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Background: Lifestyle physical activity (ie, moderate physical activity during routine daily activities most days of the week) may benefit human immunodeficiency virus (HIV)–positive adults who are at high risk for cardiovascular disease.

Objective: The aims of this study were to describe lifestyle physical activity patterns in HIV-positive adults and to examine the influence of lifestyle physical activity on markers of cardiovascular health. Our secondary objective was to compare these relationships between HIV-positive adults and well-matched HIV-uninfected adults.

Methods: A total of 109 HIV-positive adults and 20 control participants wore an ActiGraph accelerometer, completed a maximal graded cardiopulmonary exercise test, completed a coronary computed tomography, completed anthropomorphic measures, and had lipids and measures of insulin resistance measured from peripheral blood.

Results: Participants (N = 129) had a mean age of 52 ± 7.3 years, 64% were male (n = 82), and 88% were African American (n = 112). On average, HIV-positive participants engaged in 33 minutes of moderate-to-vigorous physical activity per day (interquartile range, 17–55 minutes) compared with 48 minutes in controls (interquartile range, 30–62 minutes, P = .05). Human immunodeficiency virus–positive adults had poor fitness (peak oxygen uptake [VO2], 16.8 ± 5.2 mL/min per kg; and a ventilatory efficiency, 33.1 [4.6]). A marker of HIV disease (current CD4+ T cell) was associated with reduced peak VO2 (r = −0.20, P < .05) and increased insulin resistance (r = 0.25, P < .01) but not with physical activity or other markers of cardiovascular health (P ≥ 0.05). After controlling for age, gender, body mass index, and HIV status, physical activity was not significantly associated with peak VO2 or ventilatory efficiency.

Conclusion: Human immunodeficiency virus–positive adults have poor physical activity patterns and diminished cardiovascular health. Future longitudinal studies should examine whether HIV infection blunts the beneficial effects of physical activity on cardiovascular health.

Allison R. Webel, PhD, RN Assistant Professor, Frances Payne Bolton School of Nursing, Case Western Reserve University, Cleveland, Ohio.

Joseph Perazzo, PhD, RN Postdoctoral Fellow, fellow Frances Payne Bolton School of Nursing, Case Western Reserve University, Cleveland, Ohio.

Christopher T. Longenecker, MD Assistant Professor, Harrington Heart and Vascular Institute, University Hospitals Cleveland Medical Center, Ohio.

Trevor Jenkins, MD Assistant Professor, Harrington Heart and Vascular Institute, University Hospitals Cleveland Medical Center, Ohio.

Abdus Sattar, PhD Assoicate Professor, School of Medicine, Case Western Reserve University, Cleveland, Ohio.

Margaret Rodriguez Student Research Assistant, Frances Payne Bolton School of Nursing, Case Western Reserve University, Cleveland, Ohio.

Nate Schreiner, PhD, RN Graduate Research Assistant, Frances Payne Bolton School of Nursing, Case Western Reserve University, Cleveland, Ohio.

Richard A. Josephson, MD, MS Professor, Harrington Heart and Vascular Institute, University Hospitals Cleveland Medical Center, Ohio.

C.T.L. has received honoraria from Gilead Sciences and has received research grants from Bristol-Myers Squibb and Medtronic Global Health Foundation.

This project was funded by grants from the American Heart Association (14CRP20380259) and a developmental grant from the University Hospitals/Case Western Reserve University Center for AIDS Research (National Institutes of Health grant: P30 AI036219).

The authors have no conflicts of interest to disclose.

Correspondence Allison R. Webel, PhD, RN, Frances Payne Bolton School of Nursing, Case Western Reserve University, 10900 Euclid Ave, Cleveland, OH 44106 (arw72@case.edu).

Approximately 1.2 million people are living with human immunodeficiency virus (HIV) (PLWH) in the United States, and there are more than 30 million PLWH worldwide. Human immunodeficiency virus antiretroviral therapy (ART) has significantly increased the life expectancy among PLWH.1,2 Long-term HIV infection, HIV treatment, and lifestyle factors have led to PLWH experiencing age-related comorbid conditions earlier and more frequently than HIV-uninfected individuals.3 Specifically, PLWH experience chronic inflammation, long-term use of ART, and higher rates of lifestyle risk factors that increase their risk for cardiovascular disease (CVD)3 and create an urgent need for interventions that reduce this risk.

Physical activity includes activities performed as part of daily life (eg, walking) and planned, more vigorous physical activity.4 Seminal research has shown that physical activity can improve cardiovascular and metabolic health.5 Conversely, physical inactivity is associated with poor glycemic control and reduced triglyceride clearance, resulting in an increased risk of mortality and cardiometabolic complications.6 Furthermore, PLWH also have higher rates of insulin resistance, fatigue, pain, depression, and smoking and alcohol use, compounding their risk for CVD.7–13 People are living with HIV can benefit tremendously from physical activity, but their objectively measured physical activity patterns, and the influence of those patterns on cardiovascular health, are not well understood. The aims of this study were to describe physical activity patterns in PLWH who did not meet American Heart Association–recommended guidelines for physical activity and to examine the relationship of these patterns to markers of cardiovascular health. Furthermore, we aimed to compare these relationships between PLWH and a well-matched HIV-uninfected control group.

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Methods

Design

These data were derived from a cross-sectional analysis of baseline data from a clinical trial (parent study) testing the effect of a self-management intervention on exercise and cardiovascular outcomes in a group of PLWH compared with well-matched HIV-uninfected control participants (NCT02553291).

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Sample and Recruitment

A total of 109 PLWH and 20 well-matched control participants were recruited via institutional review board–approved letters to an HIV research registry and flyers posted in HIV care organizations in Cleveland, Ohio. Human immunodeficiency virus–uninfected participants were recruited using ResearchMatch and flyers posted in primary care clinics in Cleveland, Ohio. Those interested in participating telephoned a research assistant who screened callers for eligibility. Human immunodeficiency virus–uninfected participants were matched to PLWH on race, gender, and age (±3 years). All participants had to be older than 18 years and at high risk for developing CVD (Framingham 30-year CVD risk score: >20% for females and >30% for males). If prescribed a statin medication, participants had to be taking it for at least 6 months. In addition, PLWH had to be on ART with suppressed HIV-1 viremia (<400 copies/mL) for at least 1 year before enrollment. Potential participants were excluded if they (1) had a medical contraindication for exercise;14 (2) met weekly physical activity recommendations of 150 minutes of moderate-to-vigorous physical activity (MVPA)15 (assessed using the 7-day physical activity recall16); (3) were unable to understand spoken English, (4) expected to move out of the immediate area, have surgery, or were pregnant or planned on becoming pregnant in the next 6 months; (5) were diabetic (HgA1C > 7%); or (6) were enrolled in a weight loss program.

Eligible participants were invited to an initial visit where study staff reviewed study purpose, procedures, risk, and potential benefits with them. After confirming understanding, those wishing to proceed signed an informed consent document, completed a blood draw, and if a woman of childbearing age, completed a urine pregnancy test. The institutional review board at University Hospitals, Cleveland Medical Center, approved this study.

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Procedures and Measures

Demographics and Human Immunodeficiency Virus Characteristics

All participants completed a self-reported demographic survey assessing gender, race, education, and monthly income.17 A research assistant helped those who were unable to complete the self-administered computer survey. Participants also consented to medical chart abstraction from which study staff abstracted medical data including years living with HIV and current CD4+ T-cell count and CD4+ T-cell nadir.

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Physical Activity

Participants were given an ActiGraph GT3X/+ accelerometer (ActiGraph, LLC, Fort Walton Beach, Florida).18–20 Participants were instructed to wear the accelerometer during all waking hours for 7 consecutive days, except for when showering and swimming. A research assistant affixed the monitor to adjustable elastic belts and placed it over the participant's nondominant hip and counseled the participant on the importance of wearing it every day. A research assistant called each participant 2 days after they received the devices to check if they were wearing them correctly, address concerns, and remind them to return it in 1 week. When participants returned the accelerometer, we checked to ensure that data met the minimum quality standards (at least 3 days and at least 10 hours per day).21–23 Those not meeting standards were asked to rewear it for 7 days. Accelerometer data were processed according to recommendations for adults and were sampled at 30 Hz, using 60-second epochs and the normal filter.24 Consistent with Caspersen et al's25 definition, activity of 2 metabolic equivalents or higher and 10 minutes or more was defined as exercise. We used the ActiLife software to calculate the amount of time spent in light physical activity, moderate physical activity, vigorous physical activity, and MVPA per valid day using the Freedson et al's26,27 adult calculation.

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Blood Pressure and Body Mass Index

Participants were escorted to a clinical research unit where trained research nurses measured their height, weight, and vital signs. Each participant's height was measured to the nearest 0.1 cm by asking him/her to stand straight up against a stadiometer platform with shoes off. After removing everything but a light layer of clothing, the participant stepped on a scale and weight was measured to the nearest kilogram. Body mass index (BMI) was calculated by dividing weight in kilograms by height in meters squared.

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Cardiovascular Health

Our measures of cardiovascular health included cardiorespiratory fitness, cardiometabolic health indicators (see serum laboratory measures), and cardiac computed tomography (CT) scans. Cardiopulmonary exercise tests were performed using a computer-controlled Lodi bicycle ergometer (Groninger, Netherlands) with an MGC Diagnostics Cardiopulmonary Express system (MGC Diagnostics, St Paul, Minnesota). A trained investigator performed all of the tests using a 20-W/min ramp protocol. We measured cardiorespiratory fitness using a peak oxygen uptake (VO2) measure. Peak VO2 was defined as the maximal value of VO2 during the final 30 seconds of exercise. The Wasserman-Hansen equation28 was used to determine the percent of predicted peak VO2. Ventilatory efficiency (ventilation [VE]/VCO2 slope) was determined by the linear regression slope of the minute VE and VCO2.29 Anaerobic threshold was manually calculated using the Beaver-Wasserman V-slope method.30

All participants underwent a noncontrast CT scan of the chest for coronary artery calcium scoring. A single-reader (blinded to treatment assignment and participant characteristics) quantified total coronary calcium score using the Agatston et al's31 method. All scans were performed on a 64-slice multidetector CT scanner (Somatom Sensation 64, Siemens Medical Solutions) with 30-×-0.6–mm collimation, 330-millisecond rotation time, and 120-kV tube voltage. Three-millimeter slices were obtained from the carina to the diaphragm with prospective electrocardiogram gating at 60% of the R-R interval. Calcified coronary lesions were defined as areas of 6 pixels or more with density of higher than 130 Hounsfield units.

Serum Laboratory Measures: Serum studies were used to evaluate cardiometabolic health indicators and inflammation. All participants underwent a 12-hour fasting blood draw at the clinical research unit where a trained phlebotomist drew approximately 20 mL of blood. Serum measures of HgA1C, glucose, insulin, and high sensitivity C-reactive Protein were analyzed fresh samples using standard clinical procedures and commercially available assays at the hospitals laboratory. We used participants' fasting glucose and insulin measures to calculate the homeostatic model assessment of insulin resistance for each individual.32 Interleukin (IL)-6 levels were measured in batch from plasma stored at −80°C using the IL-6 Quantikine HS ELISA Kit from R&D Systems, Inc (Minneapolis, Minnesota). All assays were conducted according to the manufactures' instructions.

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Data Analysis

All statistical analyses were performed using Stata version 14.0 (College Station, Texas). Data were cleaned and met assumptions for inferential statistics. We analyzed demographic, HIV, physical activity, and cardiovascular health characteristics by decade of age and HIV status. Categorical variables were summarized using frequencies and percentages. Continuous variables, depending on their distribution, were summarized with either means and SDs or medians and interquartile ranges (IQRs). We used Pearson's correlation coefficient to analyze the relationships between physical activity and cardiovascular health, as well as HIV biomarkers in the PLWH. We used adjusted linear regression to identify independent associations between physical activity, cardiovascular health indicators, and HIV status. We adjusted for clinically relevant covariates known to influence these relationships, including age, gender, BMI, and IL-6.33

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Results

Demographics and Human Immunodeficiency Virus Characteristics

A total of 109 PLWH and 20 well-matched HIV-uninfected participants were enrolled in the study. Among PLWH, 70 (64%) were male, 94 (86%) were African American, 56 (51%) had a high school degree or less education, and 9 (8%) were employed. People living with HIV were less likely to be employed (8% vs 35%), were engage in less moderate daily physical activity (33.3 vs 47.8 minutes), had less VE/VCO2 (33.1 vs 30.2), and had a lower systolic blood pressure (124 vs 132 mm Hg), compared with the controls. Otherwise, there were no statistically significant differences between the 2 groups. Demographic, HIV, and inflammatory characteristics are summarized in Table 1.

TABLE 1

TABLE 1

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Physical Activity

A total of 90 PLWH (83%) and 19 control (95%) participants engaged in any MVPA in the past week. The median engagement in MVPA per day was 35.1 minutes (IQR, 18–58 minutes) in PLWH and 55.2 minutes (IQR, 31–65 minutes; P = .06) in controls. Nearly all physical activity was done at moderate intensity.

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Cardiovascular Health

The average peak VO2 achieved for PLWH was 16.8 ± 5.2 versus 16.9 ± 5.9 mL/kg per minute for the control group. The VE/VCO2 for PLWH was 33.1 (4.6) compared with 30.2 (2.5) for the control group. In contrast to exercise, peak VO2 achieved did not change with age (Figure 1). Forty PLWH (36%) had a coronary calcium score greater than 1 compared with 8 (40%) in the control group (Table 1). Among PLWH, step counts were associated with decreased IL-6 (r = −0.266, P < .05), improved peak VO2 (r = 0.342, P < .05), and reduced insulin resistance (r = −0.215, P < .05). There were no other associations between physical activity and markers of cardiovascular health.

FIGURE 1

FIGURE 1

Current CD4+ T-cell count and CD4+ T-cell nadir are important health indicators for PLWH but were not associated with physical activity. However, current CD4+ T-cell count was associated with reduced peak VO2 (r = −0.199, P < .05) and elevated insulin resistance (r = 0.248, P < .05) (Table 2).

TABLE 2

TABLE 2

The regression analyses indicated that (controlling for age, gender, BMI, and IL-6) physical activity was not significantly associated with peak VO2 (overall model adjusted R2 = 0.42, P < .01), peak VE/VCO2 (Table 3), or coronary calcium score (not shown). However, PLWH exhibited less VE/VCO2 slope than controls, and our interaction coefficient (β = −1.944, P = .317) suggests that physical activity may help to mitigate this decreased VE/VCO2 slope (Table 3).

TABLE 3

TABLE 3

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DISCUSSION

Our study is among the first to prospectively examine the relationships between objectively measured lifestyle physical activity and cardiovascular health in PLWH compared HIV-uninfected controls. We produced several important findings in this study: (1) PLWH engaged in low amounts of physical activity, (2) PLWH achieved low levels of peak VO2 and elevated levels of VE/VCO2 suggesting that HIV may attenuate the effects of physical activity on cardiovascular fitness, and (3) HIV biomarkers (CD4+ T cells and CD4+ T-cell nadir) were not associated with physical activity but were associated with peak VO2 achieved. Furthermore, because our sample was largely African American, our work provides evidence that should be considered when developing targeted interventions to this high-risk and often underserved group.

Although PLWH engaged in a median of 35 minutes of moderate activity per day, exceeding daily American Heart Association recommendations, almost no one who engaged in vigorous activity suggesting that this is not exercise but rather activity conducted in the course of their activities of daily living. Our results are similar to those in a recent meta-analysis conducted by Vancampfort et al.34 The authors examined self-reported physical activity levels using metabolic equivalent minutes per week in 3780 PLWH.34 They found that PLWH engaged in mostly light activity (72.8 min/wk), followed by moderate (61 min/wk) and vigorous (12.4 min/wk) activity. Approximately 50% of PLWH met recommended physical activity levels (≥150 min/wk of MVPA), and no comparisons were made to controls.34 Conversely, in the Multicenter AIDS Cohort Study,35 physical activity levels of PLWH and uninfected controls (n = 1,281) were measured using the International Physical Activity Questionnaire.36 Comparing Vancampfort et al's34 with our results, they found that PLWH engaged in higher levels of MVPA and physical activity behaviors were similar to controls.35 Among Multicenter AIDS Cohort Study participants, HIV infection and low levels of physical activity were associated with higher insulin resistance, further demonstrating the importance of physical activity to cardiometabolic health in PLWH.35,37

Our results build on previous research by providing both objectively measured physical activity and a well-matched comparison group. The total amount of MVPA that our participants engaged in was approximately 30% less than that reported by controls or by MVPA totals in Vancampfort et al's (2016) review. There are several possible explanations for our comparatively low level of physical activity. First, by using an ActiGraphs, we minimized the risk of overreporting and behavior change bias associated with visual feedback seen in other wearable devices.38 Second, we enrolled participants who did not meet physical activity recommendations to target those most likely to benefit from an intervention. This may have blunted the overall amount of observed physical activity. However, of the 204 participants screened for this study, only 10 were excluded because they exceeded weekly physical activity recommendations. It is possible that, although low, the physical activity patterns observed in our study may be reflective of the PLWH ages 40 years and older. Finally, our sample is older than those previously analyzed, and physical activity levels decrease as PLWH age, highlighting the need for increased physical activity interventions in older PLWH.

Given these low levels of physical activity, it was unsurprising to find that some cardiovascular parameters of health were lower in PLWH compared with healthy controls. The peak VO2 achieved for all PLWH was 16.8 ± 5.2 mL/min per kg and the VE/VCO2 was 33.1, indicating impaired carbon dioxide removal and a higher risk for heart failure–related mortality.39 Peak VO2 declined and VE/VCO2 increased with age. Similarly, Vancampfort et al40 found that the average peak VO2 among PLWH was 26.4 mL/min per kg, among the lowest levels of those living with chronic diseases. Furthermore, the average VO2 peak among healthy adults (ages 40–59 years) was 34 mL/min per kg,41 significantly higher than that of our observed values. These data suggest that PLWH have poor cardiovascular fitness, which may underlie much of the increased CVD burden experienced by this population. These data also illustrate the critical importance of assessing cardiovascular fitness in this population, both clinically and as a research variable.42

Cardiovascular health can be improved through regular moderate-to-vigorous lifestyle physical activity. Recently, O'Brien et al10 found that combined aerobic and resistance interventions at least 3 times per week for at least 5 weeks can significantly improve cardiorespiratory fitness (peak VO2 Δ ≥ 2 mL/min per kg). However, studies testing home-based interventions among PLWH have largely been unsuccessful, failing to produce meaningful change in physical activity in this population.43–45 This suggests that these interventions were not well targeted to PLWH. Additional rigorous developmental research is needed to better understand how to improve physical activity in this population.

Finally, we observed a relationship between CD4+ T-cell count and peak VO2 (r = −0.199, P < .05). This finding is in contrast to recent studies that have investigated cardiovascular fitness variables and markers of HIV. In O'Brien et al's (2016) meta-analysis, for example, 5 experimental studies examined peak VO2 and markers of HIV, including CD4 T-cell count, nadir CD4 count, and HIV viral load. Consistently, studies showing improved peak VO2 in PLWH had relative stability in markers of HIV. No direct relationship between these variables was observed. However, indirect relationships between these variables have been documented, particularly those related to chronic inflammation experienced by PLWH.34 Our results showed that PLWH had higher levels of the inflammatory cytokine IL-6 compared with controls and that elevated IL-6 levels were associated with fewer step per day and diminished peak VO2 in PLWH. Although inflammation is not unique to PLWH, HIV infection results in a state of elevated inflammation, particularly when HIV is poorly controlled. As such, higher levels of inflammation experienced by PLWH may play a role in their inability to achieve a similar peak VO2 to controls. This may occur because elevated IL-6 is associated with increased fatigue, limiting how much PLWH can engage in physical activity and exercise. However, recent evidence suggests that physical activity may lead to decreased levels of inflammation,46,47 which may, in part, account for improved peak VO2 among PLWH who exercise. This evidence suggests that there is a complex interplay between factors that influence HIV disease progression and its ultimate impact on cardiovascular health.

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Limitations

Our study has several strengths including prospective data collection using objective measures of physical activity and cardiovascular fitness. However, we have several noteworthy limitations. First, as a cross-sectional study, we were unable to infer causality. Second, this is a single-site study, and although we found novel, statistically significant relationships, our findings should be examined in a representative multisite sample before implementing clinical changes based on our findings. Finally, although consistent with other studies, our results may reflect low levels of physical activity related to aging, as many of our participants were older adults living with HIV.

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Conclusion

Increasingly, PLWH are aging and developing CVD. Given the complexities of HIV disease, nonpharmacological strategies to mitigate this CVD risk are needed. Physical activity is an evidence-based strategy known to prevent CVD. Our data demonstrate that aging PLWH have poor physical activity patterns and diminished cardiovascular health. Increasing the amount and intensity of lifestyle physical activity is likely to improve aspects of cardiovascular health in this population, especially cardiovascular fitness. However, the relationship between physical activity and cardiovascular health is complex and warrants further study.

FIGURE 2

FIGURE 2

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What's New and Important

  • Physical activity levels should be regularly assessed in the clinical setting in patients living with HIV, as sedentary behavior increases their risk for CVD.
  • People are living with HIV, particularly older African Americans, may need to exercise more frequently and intensely to overcome the effects of HIV on their cardiovascular health.
  • Wearable devices are cost effective and can be used to objectively assess and evaluate physical activity of individuals at high risk for CVD.
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Keywords:

cardiovascular diseases; exercise; exercise test; HIV

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