Exercise training decreases intercostal and transversus abdominis muscle blood flows in heart failure rats during submaximal exercise

https://doi.org/10.1016/j.resp.2021.103710Get rights and content

Highlights

  • Heart failure rats were randomized to exercise-trained (ET) or sedentary groups.

  • During exercise, diaphragm muscle blood flows (BF) were not different between groups.

  • Intercostal and transversus abdominis BFs were lower in the ET group with exercise.

  • The lower respiratory muscle BFs with ET was likely via a reduced ventilatory response.

Abstract

Diaphragm muscle blood flow (BF) and vascular conductance (VC) are elevated with chronic heart failure (HF) during exercise. Exercise training (ExT) elicits beneficial respiratory muscle and pulmonary system adaptations in HF. We hypothesized that diaphragm BF and VC would be lower in HF rats following ExT than their sedentary counterparts (Sed). Respiratory muscle BFs and mean arterial pressure were measured via radiolabeled microspheres and carotid artery catheter, respectively, during submaximal treadmill exercise (20 m/min, 5 % grade). During exercise, no differences were present between HF + ExT and HF + Sed in diaphragm BFs (201 ± 36 vs. 227 ± 44 mL/min/100 g) or VCs (both, p > 0.05). HF + ExT compared to HF + Sed had lower intercostal BF (27 ± 3 vs. 41 ± 5 mL/min/100 g) and VC (0.21 ± 0.02 vs. 0.31 ± 0.04 mL/min/mmHg/100 g) during exercise (both, p < 0.05). Further, HF + ExT compared to HF + Sed had lower transversus abdominis BF (20 ± 1 vs. 35 ± 6 mL/min/100 g) and VC (0.14 ± 0.02 vs. 0.27 ± 0.05 mL/min/mmHg/100 g) during exercise (both, p < 0.05). These data suggest that exercise training lowers the intercostal and transversus abdominis BF responses in HF rats during submaximal treadmill exercise.

Introduction

A hallmark characteristic of the heart failure (HF) syndrome is impaired exercise capacity. The underlying pathophysiological mechanisms responsible for this exercise limitation are multifactorial but include impaired cardiac output and exaggerated sympathetically-mediated vasoconstriction, consequently impairing locomotor muscle blood flow (BF) (Poole et al., 2012). HF patients also exhibit pulmonary system abnormalities at rest and during exercise (e.g., obstructive-resistive lung disorders, increased physiologic dead space, and ventilation/perfusion mismatch) (Olson et al., 2006; Poole et al., 2012; Smith and Olson, 2019). Further, HF patients exhibit an exaggerated ventilatory response, work of breathing, and subsequent respiratory muscle (i.e. diaphragm) BF response during submaximal exercise (Cross et al., 2012; Musch, 1993; Smith et al., 2018, 2017a; Smith and Olson, 2019). The reduced cardiac output reserve coupled with the elevated diaphragm BF in HF has important implications regarding cardiac output distribution during exercise (Borghi-Silva et al., 2008; Olson et al., 2010; Smith et al., 2020). Specifically, experimentally unloading the respiratory muscles in HF patients during submaximal exercise elicits decreases in leg vascular resistance and increases in leg BF, culminating in improvements in exercise tolerance (Borghi-Silva et al., 2008; Olson et al., 2010; Smith et al., 2020). Thus, therapeutic interventions aimed at unloading the respiratory muscles have the potential to mitigate the potential cardiac output redistribution from the locomotor to the respiratory muscles during submaximal exercise.

Exercise training is a clinically relevant treatment strategy (e.g., cardiac rehabilitation) that elicits beneficial pulmonary system adaptations in patients with HF (Hirai et al., 2015). Specifically, exercise training in HF with reduced ejection fraction (HFrEF) improves lung diffusing capacity, pulmonary gas exchange efficiency, and respiratory muscle strength (Adamopoulos et al., 2014; Guazzi et al., 2004; Winkelmann et al., 2009). Further, the ventilatory response during submaximal exercise at the same absolute workload is attenuated following exercise training in HF (Coats et al., 1992; Sullivan et al., 1989). It is unclear, however, if these exercise training-induced adaptations (particularly the attenuated ventilatory response) reduce the respiratory muscle metabolic requirement and subsequent BF response during submaximal exercise in HF. Therefore, the purpose of the present study was to determine the impact of exercise training on respiratory muscle (diaphragm, intercostal, and transversus abdominis) BFs and vascular conductances (VC) in HF rats during submaximal exercise at the same absolute workload. We hypothesized that diaphragm BF and VC would be lower in exercise-trained HF rats relative to their sedentary counterparts.

Section snippets

Ethical approval

The present study focuses on the impact of exercise training on respiratory muscle BF in HF rats in which a subset of these HF rats was used in a previously published investigation (Hirai et al., 2018). In the previously published investigation, young adult male Sprague-Dawley rats received a myocardial infarction (MI) under aseptic conditions as previously discussed (Hirai et al., 2018; Musch and Terrell, 1992), resulting in rats with moderate HF as indicated by heart morphometrics. The

Body weight and heart morphometrics

Body and diaphragm weights, heart morphometrics, and V̇O2max for HF + Sed and HF + ExT are shown in Table 1. Body weight and V̇O2max were higher for HF + ExT compared to HF + Sed (all, p < 0.05). Infarct size was greater for HF + Sed than HF + ExT (p < 0.05). No differences were present in diaphragm or lung weight ratios to body weight, LVEDP, or LV dP/dt between the HF + Sed and HF + ExT groups (all, p > 0.05). The lung weight ratio to body weight, LVEDP, and LV dP/dt in both groups are

Major findings

The present investigation is the first to determine the effect of exercise training on respiratory muscle BFs in HF rats during submaximal exercise. In contrast to our hypothesis, diaphragm BFs and VCs were not different between the HF + Sed and HF + ExT groups during exercise. However, we found that the HF + ExT had lower intercostal and transversus abdominis BFs and VCs than HF + Sed during submaximal exercise. These results indicate that exercise training can attenuate intercostal and

Funding

This work was supported by the National Institutes of Health (HL-2-108328 to DCP, T32 HL07111 to JRS, and K12 HD065987 to JRS), American Heart Association (Grant-in-Aid 10 GRANT 4350011 to DCP), Kansas State University College of Human Ecology (Postdoctoral Fellowship to DMH), and Purdue University (EVPRP PRF Faculty Grant to DMH). This work was also supported by grants from the National Institutes of Health, National Institute of General Medical Sciences, IDeA Networks of Biomedical Research

Declaration of Competing Interest

The authors report no declarations of interest.

References (33)

  • S.W. Copp et al.

    Progressive chronic heart failure slows the recovery of microvascular O2 pressures after contractions in the rat spinotrapezius muscle

    Am. J. Physiol. Heart Circ. Physiol.

    (2010)
  • M.L. Crosfill et al.

    Physical characteristics of the chest and lungs and the work of breathing in different mammalian species

    J. Physiol.

    (1961)
  • T.J. Cross et al.

    The resistive and elastic work of breathing during exercise in patients with chronic heart failure

    Eur. Respir. J.

    (2012)
  • M.D. Delp et al.

    Changes in skeletal muscle biochemistry and histology relative to fiber type in rats with heart failure

    J. Appl. Physiol. (1985)

    (1997)
  • E.R. Diederich et al.

    Dynamics of microvascular oxygen partial pressure in contracting skeletal muscle of rats with chronic heart failure

    Cardiovasc. Res.

    (2002)
  • C. Dunham et al.

    Effects of high-intensity interval training on pulmonary function

    Eur. J. Appl. Physiol.

    (2012)
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