Respiratory Muscle Warm-Up Its Role in Enhancing Exercise and Pulmonary Functions

RESPIRATORY MUSCLE WARM-UP: ITS ROLE IN ENHANCING EXERCISE AND

PULMONARY FUNCTIONS

Chapter 1. Introduction

1.1 Purpose

The purpose of this review is to identify the value of a specific respiratory warm-up on

exercise performance and the respiratory system, particularly the respiratory muscles and

bronchial airways in healthy individuals. Many exercise physiologists believe that the respiratory

system has little to no effect on limiting exercise performance in healthy individuals or athletes

(A. McConnell, 2009), yet the respiratory system encounters several challenges during intense

exercise. One example is that the regulation of alveolar partial pressure of oxygen (O2) and

carbon dioxide, achieved by a considerable increase in alveolar ventilation, minute ventilation

(VE), often 20 times the resting value in humans. This is achieved by the capacity of the

respiratory muscles to not only generate force to alveolar ventilate but also by limiting excessive

physiological cost on the system during exercise (Guenette & Sheel, 2007). A second example of

the challenges the respiratory system must overcome is the ability of the bronchial (intra-

thoracic) airways to maintain patency to allow the increase flow rate needed during active

expiration often seen in intense exercise. During high intensity exercise, the bronchial airways

occasionally do present a significant limitation to expiratory flow, thereby causing dynamic

hyperinflation, increased respiratory muscle work, and VE limitation (Forster, Haouzi, &

Dempsey, 2012). Research has focused on these functions (muscular work/fatigue and airway

patency) of the respiratory system to determine respiratory limitation during and after exercise.

A review of these areas of function will follow, as well as possible ways to overcome and/or

lessen the challenges imposed on the respiratory system during exercise.

This review has four sections. The first will serve as an overall introduction to factors

relevant to this review of the respiratory system during and following exercise, exercise induced

bronchoconstriction (EIB)/exercise induced asthma (EIA), and an examination of expiratory

flow limitation (EFL). The second will examine methods to train the respiratory system for

exercise performance. The third will examine the use of various types of warm-up that may be

used to take advantage of a so-called “refractory period.” The final section will discuss the future

direction of research based on the areas identified during this review.

1.2 Respiratory System: Challenges with Exercise

For the purposes of insight to the control of breathing mechanisms as seen during

exercise, one should review the information found in Forster et al. (2012) and others like Babb,

Wood, and Mitchell (2010) and Miyamoto (1990). The mechanical work necessary to ventilate

the lungs at rest and during exercise has many mechanisms to involve elastic and non-elastic

work with some sub-components including inertial forces, gravitational forces, and distortional

forces of the chest wall (Guenette & Sheel, 2007). During heavy exercise, additional mechanical

constraints are placed on the respiratory system’s ability to increase VE, including the capacity

of the inspiratory muscle pump to generate negative pleural pressure and the capacity of the

intra-thoracic airways to maintain patency that allows for increases in flow rates during active

expiration (Forster et al., 2012). The total mechanical work is the sum of all of these factors. An

increase in VE with progressive exercise to exhaustion creates a disproportionate increase in

mechanical work and the O2 cost of breathing. However, in cases of healthy individuals, the

dynamic capacity of the inspiratory/expiratory muscles for force generation probably never

limits the VE response to exercise (Guenette & Sheel, 2007). More specifically, only about one-

half of the inspiratory muscle’s dynamic capacity is reached at peak exercise in young adults. As

much as 80-90% of the inspiratory muscle’s dynamic capacity needed by highly trained athletes

to generate the required intra-pleural pressures requires twice the metabolic cost (O2) and VE

responses as that seen in untrained individual (Forster et al., 2012).

An often-overlooked ingredient to possible limitation is how the mechanical work of

breathing has both sensory and metabolic repercussions. The perceived work of breathing

contributing to how hard the exercise feels and the demands the mechanical work of breathing

places on the circulatory system for blood (O2) to sustain muscle contraction are examples of the

sensory and metabolic consequences (A. McConnell, 2009). It has been suggested that the

metabolic and circulatory cost of a high mechanical work of breathing during maximal levels of

VE can amount to 8-10% of the VO2max and cardiac output in the untrained individual and up to

14-16% of VO2max and cardiac output in highly-trained individuals (Aaron, Johnson, Seow, &

Dempsey, 1992; Harms, McClaran, et al., 1998). These findings may represent the respiratory

system’s inability to sustain airway patency in the face of maximal or near maximal workloads,

creating high VE demands and variations in possible expiratory muscle fatigue because of

changes in dynamic hyperinflation seen in EFL.

The primary muscle of active inspiration in humans is the diaphragm. The diaphragm is a

large, dome-shaped muscle separating the abdominal and thoracic cavities and innervated by the

phrenic nerve. It possesses unique characteristics that make it the most fatigue resistant (very

high aerobic enzymatic capacity, rich sources of blood supply, and resistant to vasoconstriction)

of all the skeletal muscles (Miller, Hemauer, Smith, Stickland, & Dempsey, 2006). Other

muscles that can assist the diaphragm with inspiration are the external intercostal, scalene, and

sternocleidomastoid (accessory muscles). As ventilation increases the respiratory muscles are

recruited. During quiet breathing, there is little or no muscle contraction/relaxation involved in

expiration, and the elastic recoil of the lungs in healthy individuals drives the process. The

abdominal muscles and the internal and innermost intercostal muscles assist forced or active

expiration that occurs during heavy intensity exercise (Guenette & Sheel, 2007). The recruitment

of the diaphragm during exercise may be assessed indirectly through measurement of trans-

diaphragmatic pressure (Pdi), surface electromyography (EMG), and use of bilateral phrenic

nerve stimulation (BPNS) with Pdi. Pdi is the measured difference between gastric and

esophageal pressure and can be assessed during BPNS (a bilateral and supra-maximal

stimulation of the phrenic nerve via electrical/magnetic stimulation) (Guenette & Sheel, 2007;

Johnson, Babcock, Suman, & Dempsey, 1993). From research using these techniques, it is

believed the diaphragm is recruited in proportion to the increases in VE with increasing intensity

of exercise (Johnson et al., 1993). Others have proposed that the Pdi plateaus in the face of

increasing VE, thereby suggesting that accessory muscle recruitment plays an active part in the

total pressure generated by the inspiratory muscles (Johnson et al., 1993). Regardless of the

contribution of the diaphragm and the accessory muscles, the force output required to sustain

VE during intense exercise requires significant muscle work (O2 demand) and a significant

proportion of the cardiac output to meet the applied intensity. Considering the factors of high O2

demand, required cardiac output, and high work of breathing, it seems plausible that the

diaphragm and accessory muscles may be susceptible to fatigue (Guenette & Sheel, 2007).

Fatigue in respiratory muscles is a condition in which there is a reduction in the capacity for

developing force and/or velocity of a muscle, which is caused by activity under load and which

is reversible by rest (Macklem, 1990; "NHLBI Workshop summary. Respiratory muscle

fatigue. Report of the Respiratory Muscle Fatigue Workshop Group," 1990). The diaphragm

will show significant fatigue during sustained exhaustive exercise with intensities greater than

80-85% of VO2max (Johnson et al., 1993; Miller et al., 2006). Exercise-induced diaphragmatic

fatigue is caused by high levels of diaphragmatic work that must be sustained throughout high-

intensity exercise. With prolonged high intensity exercise, hyperventilation is present

throughout,

suggesting that diaphragmatic fatigue does not impede the ventilator response (Miller et al.,

2006). However, indirect evidence of pressure readings suggests that the fatiguing diaphragm

reduces its force generation during the late stages of sustained endurance exercise. This causes

the accessory muscles of inspiration and the expiratory muscles to become more dominant in

maintaining respiratory muscle work and hyperventilation. This increased use of expiratory

muscles helps create a reduction of end-expiratory lung volume, which increases intra-abdominal

pressure, thus allowing the diaphragm to lengthen, preserving its maximal ability to force

generate (Forster et al., 2012). Some researchers have attempted to identify if respiratory muscle

can be fatigued.

When a proportional assist ventilator (PAV) was used during exercise, fatigue of the

diaphragm was prevented (Babcock, Pegelow, Harms, & Dempsey, 2002). These findings do

suggest respiratory muscles can be fatigued during maximal exercise. Research by Babcock et al.

(1995) evaluated resting subjects as they voluntarily mimicked the magnitude and duration of

diaphragmatic work seen during endurance exercise. They noted that fatigue did not occur until

diaphragmatic work increased to double the work required during maximal exercise. This would

suggest that the diaphragm must compete with the loco-motor muscles for the available cardiac

output during heavy-intensity exercise, leaving the diaphragm with inadequate O2 transport,

thereby creating a fatigued state (Miller et al., 2006). This fatigued state likely activates meta-

boreflexes from within the inspiratory and expiratory muscles, which increase sympathetic

vasoconstrictor outflow, leading to a redistribution of cardiac output (Harms, McClaran, et al.,

1998).

There are complex mechanical effects of intra-thoracic and intra-abdominal pressure on

stroke volume and cardiac output with respiratory muscle fatigue (Forster et al., 2012). EFL is

accompanied by high expiratory pressures, which may approach or exceed the critical closing

pressure of the airways with exercise, which can result in increased left ventricular afterload and

reduced stroke volume (Miller, Pegelow, Jacques, & Dempsey, 2005). If inspiration is

accomplished by the diaphragmatic contraction alone, then the resulting increase in intra-

abdominal pressure with the downward movement of the diaphragm impedes the exercising

lower limb venous return (Forster et al., 2012). Miller et al. (2005) suggests that this reduced

venous return is recovered during expiration with little net effect on reduced total venous return.

As reviewed earlier, during heavy sustained exercise, respiratory muscle blood flow may

consume 8-10% of the VO2max and cardiac output in the untrained individual and up to 14-16%

of VO2 and cardiac output in highly trained individuals, thus affecting blood flow for the

working limb muscles (Aaron et al., 1992; Harms, McClaran, et al., 1998; McClaran, Harms,

Pegelow, & Dempsey, 1998).

Harms et al. (1998) set out to test the effect of respiratory muscle fatigue on sympathetic

outflow vs. exercising limb blood flow by altering the work of breathing during high intensity

cycling exercise. They used resistive loading and a PAV unloading of the respiratory muscles to

manipulate the work of breathing. Their results suggest that exposure of the respiratory muscle

to a loaded state produced a reflex vasoconstriction reducing blood flow to the exercising limb.

Conversely, when the respiratory muscles were unloaded with the PAV, a state of increased

blood flow (dilation) existed. These changes in limb blood flow indicate a competitive

relationship exists between the muscles of locomotion and the muscles of respiration for limited

cardiac output (Guenette & Sheel, 2007). Research on time to exhaustion (performance) using

the same loading and unloading of the respiratory muscles as discussed above showed that

loading via resistive devices produced a decrease in time to exhaustion and unloading with a

PAV increased time to exhaustion averaging ±14-15% (Harms et al., 2000). These results

suggest that increased performance (time to exhaustion) effect may be explained with reduced

dyspnea perceptions secondary to reduced respiratory muscle work (Miller et al., 2006).

The respiratory system must contend with many challenges during exercise. The most notable

challenge is the mechanical work of the respiratory muscles because of the necessity to ventilate

the lungs at rest and during exercise and the capacity of the intra-thoracic airways to maintain

patency that allow for increases in flow rates during active expiration. During exercise the

increase in VE with progressive exercise to exhaustion creates a disproportionate increase in

mechanical work (as listed above), hence an increase in O2 cost of breathing. This increase O2

cost from mechanical work to achieve increase in VE during heavy sustained exercise creates

competition for cardiac output, thereby affecting blood flow for the working limb muscles and,

thus, causing fatigue in both muscle groups (respiratory muscle and working skeletal limb

muscles). Could exercise performance be enhanced if the challenges placed upon the respiratory

system were reduced by changing the pre-exercise condition of the same respiratory system?

1.3 Exercise and the Effects on Pulmonary Function

The second described challenge facing the respiratory system during intense exercise is

the ability of the bronchial (intra-thoracic) airways to maintain patency to allow increased flow

rate during active expiration often seen with high-intensity exercise. As discussed earlier, during

high intensity exercise, the bronchial airways occasionally do present a significant limitation to

expiratory flow, thereby causing dynamic hyperinflation, increased respiratory muscle work, and

VE limitation (Forster et al., 2012). This challenge to maintain airway patency may be assessed

using various breathing maneuvers, which will be reviewed here.

Spirometry is a simple method of assessing lung function by measuring the volume of air

that the subject can exhale from the lungs after a maximal inspiration. It is often used to

diagnose individuals with Chronic Obstructive Pulmonary Disease (COPD) and is the best way

to detect airway obstruction (Ruppel & Enright, 2012; "Spirometry for the Health Care

Provider," 2010). Specific measures derived from spirometry (directly and indirectly) include the

forced vital capacity (FVC), slow vital capacity (SVC), forced expiratory volume in one second

(FEV₁), FEV ₁/FVC ratio, forced expiratory flow 25%, 50%, 75%, 25-75% (FEF 25%, FEF

50%, FEF 75%, and FEF 25-75%), peak expiratory flow (PEF), and peak inspiratory flow (PIF)

(Ruppel & Enright, 2012). Another measure that is often performed after spirometry is the

maximal voluntary ventilation (MVV), which can be used to derive a breathing reserve value

during maximal exercise testing (Bender & Martin, 1985; Hill, Jacoby, & Farber, 1991; Johnson,

Weisman, Zeballos, & Beck, 1999). Some other measures use different devices to assess

maximal inspiratory pressure (MIP or PImax), and maximal expiratory pressure (MEP or PEmax)

(Coast et al., 1999; Haverkamp, Metelits, Hartnett, Olsson, & Coast, 2001). A more difficult

measure because of the nature and bulkiness of the equipment needed is the determination of

total lung capacity (TLC), residual volume (RV), fraction of residual capacity (FRC), and

expiratory reserve volume (ERV) (Chapman, Allen, & Romet, 1990; Ruppel & Enright, 2012).

Recent studies have used many of these measures separately or in various combinations to assess

respiratory muscle weakness and EFL.

The most commonly used spirometry values for assessment of respiratory muscle

weakness/ fatigue and EFL have been the measures of FVC and FEV ₁(Coast et al., 1999;

Haverkamp et al., 2001; Hill et al., 1991; Mahler & Loke, 1981; O'Kroy, Loy, & Coast, 1992).

The second most commonly used measures are the MIP and MEP (Coast et al., 1999;

Haverkamp et al., 2001; Hill et al., 1991; O'Kroy et al., 1992; Ozkaplan, Rhodes, Sheel, &

Taunton, 2005). Few studies use MVV, TLC, RV, and ERV to assess EFL and possible

respiratory muscle fatigue (Bender & Martin, 1985; Cordain, Rode, Gotshall, & Tucker, 1994;

Nourry, Deruelle, et al., 2005a).

Haverkamp et al. (2001) studied the effect of expiratory muscle fatigue on pulmonary

functions in eight (seven male and one female) healthy human subjects exposed to an expiratory

fatigue (EF) trial (loaded breathing protocol). Pre and post-trial recovery (0, 5, 10, and 15-

minutes) measures were compared to a control trial (CT). The findings suggest MEP was the

only measure to see significant change between EF trial pre/post and CT that remained

unchanged. This finding is not surprising because the EF trial termination was when the MEP

value fell below 80% of the pretrial value. It also seems plausible that the EF trial was not of

significant intensity or duration (average time to trial end was seven-minutes) to elicit a change

in expiratory flow.

Hill et al. (1991) studied a group of triathletes to see what pulmonary function measures

changed during an endurance triathlon. Pulmonary functions were obtained after each event,

following the completed event, and with one day of recovery. Twelve male subjects completed

the 3.8 km swim, 180 km bike, and the 42 km run with an average finishing time of 12-hours 45-

±90 min. Following the completion of the triathlon, significant declines from baseline were

noted in the FVC (7.1%), FEV ₁(8.4%), FEF 50% (18.6 %), FEF 25-75% (15.2%), but no

change in MVV or the other FEF measures, ratio, and/or PEF. The PI max did not decline after the

swim, but decreased significantly after the bike (26%). That reduction continued after the run,

but the PE max showed no significant reduction at any time. The FEV ₁was the only to still be

considered significant the morning after (a proximally, 12-hours). These results suggest the

duration (>12-hours) of the exercise is an important variable reflective of declines in some

pulmonary function measures. It remains to be determined at what time interval these variables

return to baseline and the suspected causes of such declines.

Mahler and Loke (1981) studied pulmonary function in fifteen ultramarathon runners

before and after (10 to 15-minutes and 2.5-hours) a 80.6-100km (50 to 62.2-mile) road race with

a mean running time of 7-hours 42-minutes (in 80.6 km). The results revealed a significant post-

race decline in FVC (12.4%), FEV ₁(9.5%), FEF 50% (28.4), PEF (13.7%) with values

improving after 2.5 hours of recovery. The authors believe there are an airway obstructive

component (because of reduction in flow rates) and a respiratory muscle fatigue component

(because of recovery after rest and nourishment). These results are similar to the results obtained

by Hill et al. (1991) that supporting the value of exercise duration producing declines in

pulmonary function measures. However, this study showed a return to baseline values within 2.5

hours of recovery.

O'Kroy et al. (1992) examined the before and after (5, 10, 30 minutes) exercise pulmonay

function of nine (seven males and two females) active runners following exercise at three

different intensity and durations on a treadmill. The purpose of the study was to determine which

intensity and durations elicit changes in FVC and if these changes could be related to respiratory

muscle fatigue. The intensity and durations protocols were as follows: 1) a graded maximal test

to exhaustion (7-14 minutes duration); 2) a seven minute test at 90% of VO2max; and 3) a 30

minute test at 60% of VO2max. The MEP measure approached significance at 10 minutes posttest

with no difference observed between intensities and MIP showed no difference between both

time or intensities. FVC was different between times but not intensities and was decreased at

five and ten minutes as compared to pre-values. FEV ₁was significantly reduced at five and ten

minutes as compared to pre-values across intensities. The authors feel the data suggest a

combination of exercise duration and intensity may be needed to elicit changes in pulmonary

function after exercise and that expiratory muscle fatigue may be a factor that causes the reduced

FVC. Something worthy of bringing to attention (no mention in the article) is the FVC and

FEV ₁increased (to near significance) for the 30-minute, 60% of VO2max intensity protocol (from

Figure 1) at 30-minutes posttest, suggesting a possible aiway dialation taking place.

Coast et al. (1999) examined the effects of a maximal exercise trial (progressive maximal

cycle ergometer test) and a voluntary isocapnic hyperpnea (VIH) trial (mimicking frequency and

depth of breathing at maximal exercise) on pulmonary functions pre and post-trial (0, 5, 10, 15

minutes) from eleven (six males and five females) healthy subjects. A significant decrease in

FVC (7%) was observed immediately following the exercise trial, and the MIP (15%) remained

reduced for 15-minutes post-trial. The MEP and FEV ₁were unchanged with the exercise trial

and all four measures were unchanged in the VIH trial. The authors suggest the data indicate

pulmonary function and respiratory muscle strength may be altered following exercise but not

by a similar trial of VIH. They further suggest the exercise effects on pulmonary functions are

independent of respiratory muscle work done.

Ozkaplan et al. (2005) studied the relationship between respiratory muscle fatigue and

recovery (1, 2, 3, 4, 5, 10, and 15-minutes) using the MIP following exercise to VO2max in

moderately trained males (18) and females (16). The MIP significantly decreased equally in

males (16%) and females (15%) from pre-data and remained reduced in both genders throughout

15 minutes of recovery. The authors conclude inspiratory muscle fatigue following maximal

exercise demonstrates that same pattern of recovery in both males and females. The authors

could have used other measures to assess respiratory muscle fatigue such as FVC, FEV ₁and

PEF. It would have also been interesting to see if these pulmonary function measures would have

trended the same as MIP.

Cordain et al. (1987) researched the effects of long-term exercise on respiratory muscle

strength assessed by pulmonary function data in 101 male runners (at least one year and a

frequency of three or more days per week) aged 16-58 years. Results revealed that runners

exhibited significantly lower PEmax and significantly higher RV than the predicted values for

height and age matched normal subjects. No other measure showed significance. The authors

believe frequent consistent running may cause a non-pathological increase in RV due to

reductions in expiratory muscle strength.

Bender and Martin (1984) hypothesized that the ability to ventilate maximally is

decreased during and following exhaustive exercise. To evaluate this, they examined the

measure of MVV (in 60-seconds) during the final minute and post-exhaustive treadmill exercise

from 17 (14 male and 3 female) subjects (8 recreational athletes and 8 competitive runners).

Each trial lasted for either three to ten-minutes or 60-minute duration of exhaustive exercise.

Findings suggest the three to ten-minutes exercise duration failed to show any change in MVV.

However, the 60-minute exercise showed significantly lower MVV values in the final minute

and during the five and ten recovery intervals. The eight non-runners and the eight runners

showed lower MVV values only at ten-minutes recover. The authors suggest the capacity to

ventilate maximally declines only in long-term exhaustive exercise and the decline is most

pronounced in non-runners.

Nourry et al. (2005) studied ventilation constraints in thirteen (nine males and four

females) aerobically trained (TR) and eleven (seven males and four females) untrained (UT)

prepubescent children by measuring the maximal flow-volume loop (MFVL) at rest and the

exercise flow-volume loops (EFVL) (plotted in the MFVL) during a progressive exercise test to

exhaustion (8 to10-minute duration). The results show that TR had higher FVC and maximal

expiratory flows than UT. In addition, TR reported higher VE, ERV/FVC and dyspnea

associated with lower breathing reserve IRV/FVC and O2 saturation values (SaO2) at peak power

as compared to UT. Authors concluded that because of their higher VE level, TR subjects

present higher ventilatory constraints than UT.

The ability of the bronchial (intra-thoracic) airways to maintain patency, allowing for

increases in flow rate during active expiration, is a major challenge of the respiratory system

when the need for increased VE is required (often seen with intense exercise). This challenge in

the bronchial airways with intense exercise occasionally presents a significant limitation to

expiratory flow, thereby causing dynamic hyperinflation, increased respiratory muscle work, and

VE limitation (Forster et al., 2012). Spirometry and other measures may be used to assess the

airway before, during, and after exercise. Regardless of the techniques used to measure the

ability to maintain airway patency, most research suggests that limitations exist when exercise

duration and intensity are sufficient to create dynamic hyperinflation (caused by EFL) and/or

respiratory muscle fatigue (also possibly caused by EFL) in both males and females equally

(Ozkaplan et al., 2005). These limitations are supported by data by Cordain et al. (1987),

suggesting frequent, consistent running may cause a non-pathological increase in RV (dynamic

hyperinflation/EFL), and this increase may be caused by reductions in expiratory muscle

strength (respiratory muscle fatigue). It is also notable that research measuring increases in

ventilation in the absence of exercise as demonstrated in VIH trials suggests the exercise effects

on pulmonary functions are independent of respiratory muscle work done (Coast et al., 1999).

Lastly, when comparing these limitations on trained vs. untrained individuals, research suggests

that because

of their higher VE level, trained subjects present higher ventilatory constraints than untrained

subjects (Nourry, Deruelle, et al., 2005a).

1.4 Expiratory Flow Limitation

Exercise ventilatory limitation happens when the ventilatory output (VE) closely

approaches or matches ventilatory capacity (Babb, 2013). EFL during exercise has been

demonstrated in both males (Johnson, Saupe, & Dempsey, 1992) (Hue, Boussana, Le Gallais, &

Prefaut, 2003) and females (McClaran et al., 1998). Currently, there is no agreed way to quantify

ventilatory capacity, but some suggest the overlay of the exercise tidal flow-volume loop inside

the maximal resting flow-volume loop (Babb, 2013). However, Babb (2013) points out that just

making comparison of exercise tidal flow-volume loop with the maximal flow-volume loop

measured at the mouth to view the scale of the EFL may not tell the whole story. Others suggest

the use of FVC, FEV₁, PEF, FEF 50% and RV for a more effective ways of assessment (Beck,

Hyatt, Mpougas, & Scanlon, 1999; Buono et al., 1981; Cordain, Glisan, Latin, Tucker, & Stager,

1987; Cordain et al., 1994). Regardless of the measure, approaching EFL may start a cascade of

changes that could play an important role in creating ventilatory limitation during exercise and

exercise intolerance (Babb, 2013).

The cause of significant EFL in many endurance athletes during heavy exercise is

hyperinflation and an increase of their end-expiratory lung volume (Guenette, Witt, McKenzie,

Road, & Sheel, 2007; Johnson et al., 1992; McClaran et al., 1998). Most of these athletes had

normal airways and normal age-predicted maximal flow-volume data, but their high peak

exercise capacities created extreme demand on ventilations and flow-rates, often resulting in

EFL, hyperinflation, and reduced inspiratory capacities (Dempsey, McKenzie, Haverkamp, &

Eldridge, 2008). Some of the complications with hyperinflation in the lungs are as follows: 1)

causes a reduction in dynamic lung compliance, increasing elastic work of breathing, thereby

limiting the hyper-ventilatory response to heavy intense exercise, thus contributing to arterial

hypoxemia and worsening dyspnea; 2) compromised cardiac output and stroke volume caused

by increased afterload placed on the left ventricle by increased positive expiratory intra-pleural

pressure with this pressure often exceeding the critical closing pressure of the airway; 3) a

plateau of tidal volume at lower VE causing tachypnea; and 4) inspiratory muscle fatigue

developing because of muscles functioning at shorter than their optimal length with a faster

velocity of shorting operating at the limit of their dynamic capacity of their force generation

(Babb, Viggiano, Hurley, Staats, & Rodarte, 1991; Dempsey et al., 2008; Guenette et al., 2007;

Johnson et al., 1992; McClaran et al., 1998; Mota et al., 1999). EFL and this cascade of events

outlined are more likely to occur in young females (because of smaller lungs) (McClaran et al.,

1998) and older endurance athletes (loss of elastic recoil with normal aging) than young males

(Guenette et al., 2007). The EFL in females can be explained largely by anatomical factors that

affect the capacity to generate flow and volume during exercise as opposed to fitness related

factors (Dominelli, Guenette, Wilkie, Foster, & Sheel, 2011). For a more complete review of the

role and consequences of EFL during and after exercise, one should see the reviews in Babb

(2013) and Dempsey et al. (2008).

Guenette et al. (2007) compared the mechanics of breathing (EFL, end-expiratory lung

volume, end-inspiratory lung volume and the work of breathing) in endurance-trained athletes

(eighth males and ten females) during cycling exercise. EFL measurement was derived from

applying a negative expiratory pressure at the mouth as described in Mota et al. (1999). End-

expiratory lung volume and end-inspiratory lung volume were achieved via inspiratory capacity

maneuvers. Work of breathing was integrated by plotting the difference between esophageal and

airway opening pressure (trans-pulmonary pressure) against volume. The EFL limitation was

seen in nine females and three males in the final stage of exercise. Women had higher relative

end-expiratory lung volume, end-inspiratory lung volume, and work of breathing (two times)

than males at maximal exercise. The authors believe that EFL, end-expiratory lung volume, and

end-inspiratory lung volume may be more commonly experienced in females than in males at

maximal exercise because of smaller lung volumes and airway diameter seen in females, leading

to an increased work of breathing. These findings collectively suggest that females utilize a

greater majority of their ventilatory reserve at a higher cost of breathing than males.

Bruno et al. (1981) set out to determine and track the effect of an acute exercise bout

(continuous treadmill to exhaustion) on RV and TLC (determined by closed circuit O2 dilution

method) and other pulmonary functions measures over a 24-hour exercise recovery. They tested

twelve males before and after exercise (5, 15, 30-minutes, 1, 2, and 24-hours). The results

showed the RV significant increased by 20.8%, 16.8%, and 12.0% at 5, 15, 30 minutes of

recovery from exercise, respectively. TLC showed significance increases at five (2.7%) and 15

(2.3%) minutes recovery. Interestingly, the FVC and FEV ₁were unchanged following exercise.

It is possible the cool down protocol (3 miles per hour, 0% grade for 5 minutes) allowed these

values to approach resting values and not show any significance. However, looking at the data

(and something not mention by the authors), the FEF 25-75% measure (medium to small

airways) showed an increase 5.8% at five and 7.6% 15 minutes recovery, respectively. Could

this increase be reflective of a refractory period occurring? This was not an identified purpose of

this study, but it should raise a reasonable question in the face of increasing RV and TLC if these

increases reflect EFL.

Cordain et al. (1994) evaluated the mechanism that may be responsible for an often-

observed acute increase in RV following exercise in 12 males that performed two exercise bouts

on separate days. Subjects performed one exercise bout to maximal heart rate and one to 85% of

maximal heart rate for 20-minutes. Pulmonary function measures were obtained prior to and at

5, 15, 30, 60, and 120-minutes post exercise. Results show significant increases in RV at 5, 15,

and 30-minutes following maximal exercise and at 5 and 30-minutes after the submaximal

exercise. Maximal exercise displayed a greater change in RV as seen in the submaximal exercise

bout.

Decreases were noted in PEmax and FVC, possibly caused by decreased expiratory muscle

strength, but FEV ₁and FEF 75-85% were either unchanged or elevated. The authors addressed

this by claiming, the increased FEV ₁and FEF 75-85% suggest there was little or no small

airway compression by fluid volume shifts in the lung, as cited in their review of works. It is

once again interesting to note this may be the result of refractory in the airways following

exercise.

Babb et al. (1991) tried to determine the effect of mild-to-moderate airflow limitation on

exercise tolerance and end-expiratory lung volumes by examining nine control subjects with

normal pulmonary functions and twelve patients with mild-to-moderate air flow limitation

during progressive cycle exercise. Data revealed that patients had a reduced (69% of predicted)

VO2max as compared to controls (104% of predicted). End-expiratory lung volume was similar

at rest in both groups (53% of TLC), but the maximal exercise values of patients decreased to

45% of TLC, and controls increased to 58% of TLC. The authors propose end-expiratory lung

volume was significantly correlated to the FEV ₁and VO2max values and this relationship

suggests there is a ventilatory component to exercise capacity but that the increased end-

expiratory lung volume could impinge on cardiovascular function during exercise. Within the

discussion, the authors suggest the abnormal ventilatory response produced in the patients

because of their limited expiratory flow reserve values caused a reduction in their activities of

daily living, thereby creating a deconditioned state. Interesting to note is that the normal controls

also demonstrated some EFL at maximal exercise while still achieving their maximal predicted

heart rate.

Hue et al. (2003) aimed to investigate pulmonary functions (ten-minutes before and ten-

minutes after cycling trials) and compare them to those seen in the cycle/run succession as often

performed by triathletes. Thirteen young males participated in three exercise trials: 1) 30-

minutes of constant speed cycling followed by 20-minutes of constant speed running; 2) 30-

minutes control constant speed cycling; and 3) 20-minutes of control constant speed running.

The results for lung volumes and capacities for cycle-only trial showed significant increases in

RV, FRC, and RV/TLC ratios, but there was no significance found in the pulmonary volumes or

flows with the cycle/run or the run-only trials. Based on these findings the authors suggest

cycling exercise by itself seems to increase post-exercise pulmonary volume changes that may

lead to respiratory muscle (fatigue) alterations, and these changes may be a result of the

crouched position of cycling. Other studies have suggested cycling induced a greater decrease in

respiratory muscle endurance than running (Boussana et al., 2003; Boussana et al., 2001; Hill et

al., 1991). Looking into the data more deeply, the FEF values showed slight increases for pre-

values for the cycle/run and the run-only trials, which may suggest some airway refractoriness.

The series of events that are created by hyperinflation in the lungs can cause changes in

dynamic lung compliance increasing the elastic work of breathing, compromising cardiac output

and stroke volume, causing increased tachypnea, and inspiratory muscle fatigue, limiting

dynamic capacity for force generation (Babb et al., 1991; Dempsey et al., 2008; Guenette &

Sheel, 2007; Johnson et al., 1992; McClaran et al., 1998). Young females (because of smaller

lungs and airway diameter) and older endurance athletes (loss of elastic recoil with normal

aging) experience higher incidences of EFL than young males. Females utilize a greater majority

of their ventilatory reserve, thus significantly increasing their cost of breathing compared to

males (Guenette et al., 2007). With concern to exercise modality, it seems cycling exercise by

itself increases post-exercise pulmonary lung volume (increased RV) which may lead to

respiratory muscle (fatigue) alterations, and these changes may be a result of the crouched

position of cycling versus the upright position of running (Boussana et al., 2001; Hill et al., 1991;

Hue et al., 2003). A study by Babb et al. (1991) suggested end-expiratory lung volume was

significantly correlated to the FEV ₁and VO2max values, thus a relationship of a ventilatory

component to exercise capacity and an increase in end-expiratory lung volume could impinge on

cardiovascular function during exercise. The author also suggested this might cause a

deconditioned state (reduced activities of daily living) for individuals with an abnormal

ventilatory response because of their limited expiratory flow reserve values. In this same study,

the normal controls subjects also demonstrated some EFL at maximal exercise while still

achieving their maximal predicted heart rate. Three of the five studies reviewed here, suggests a

possibility of airway refractoriness seen in their subjects. Bruno et al. (1981) showed an increase

in the FEF 25-75% measure at five (5.8%) and 15-minutes (7.6%) recovery, suggesting some

increase in expiratory flow in the face of increasing RV and TLC values. Cordain et al. (1994)

found elevation or no change in FEV ₁and FEF 75-85% suggesting little or no airway

compression from fluid shifts in the lung. And lastly, a deeper review of Hue et al. (2003) of the

individual data revealed slight increases in the FEF measures compared to pretrial data for

cycle/run and run trials.

1.5 Exercise Induced Bronchoconstriction

Another area relevant to this review is exercise-induced bronchoconstriction (EIB). EIB

is a transient narrowing of the lower airway during and after exercise in the presence or absence

of clinically recognized asthma (Rundell, Spiering, Judelson, & Wilson, 2003; Weiler et al.,

2010). EIB is the preferred term over exercise-induced asthma (EIA) because not all individuals

with EIB have asthma. Also, in persons with asthma, exercise is not the inducer but the trigger

for bronchoconstriction (Brown, Howard, Khan, & Carmody, 2012). The mechanism of EIB is

based on two primary theories, the “osmotic theory” and the “thermal theory.” The osmotic

theory suggests high ventilation rates during exercise causing excessive water loss for the airway

surface liquid altering resident airway cell osmolality causing an inflammatory mediator release.

The thermal theory states exercise causes airway cooling, and a rapid rewarming upon cessation

of exercise leads to reactive hyperemia, edema, and obstruction (Rundell et al., 2003).

EIB is characterized as a ≥10 or ≥15 % of the reduction from pre to post exercise FEV ₁

and is generally seen in three to fifteen minutes of recovery from exercise (Gotshall, 2002;

Rundell et al., 2003). EIB is extremely common in persons with asthma (80-90%) and seen more

frequently in individuals with more severe cases and in poorly controlled asthma as compared to

only about 12-19% of the general population (Brown et al., 2012; Gotshall, 2002). About 40-

50% of the individuals with asthma may exhibit a “refractory period,” (diminished

bronchoconstriction to exercise if performed with 2-4 hours of first exercise) (Gotshall, 2002;

Mahler, 1993; Randolph, 1997). The use of warm-up to induce a refractory period to limit the

severity of EIB certainly can have merit for reducing symptoms, reducing the use of medications,

and increasing exercise performance (Stickland, Rowe, Spooner, Vandermeer, & Dryden, 2012).

EIB in elite athletes is generally higher than in the general population and varies based on the

type of sport, the maximum exercise level and certain environmental conditions (Brown et al.,

2012). Khan (2012) displays the prevalence (percentage) of asthma occurrence in Olympic

sports as cited in (Weiler, Layton, & Hunt, 1998; Weiler & Ryan, 2000) as follows: (60.7%)

nordic-combined, cross-country, and short track; (50%) cycling and mountain biking; (29.6%)

synchronized swimming and swimming; (24%) canoe/kayak, rowing and sailing/yachting,

and alpine, long track, figure skating, snowboarding, and curling. These athletes indicated via

a questionnaire, “They had been told either they had asthma” or “they had taken asthma

medication at some time.”

Rundell et al. (2003) set out to determine whether bronchoconstriction occurs during an

interval-type simulated cross-country ski race and whether there is a period of refractoriness

when a second bout of interval type exercise is initiated within 20-minutes post completion of

the first session. They examined airway response and refractoriness during an approximate 42-

minute cross-country ski time trial preceded by a six to nine-minute 2.5 km high intensity warm-

up ski. Eighteen (thirteen males and five females) elite cross-country skiers completed seven

successive 2.5km loops and had spirometry measured pre and at 5, 10 and 15-minutes post loop

1 and 20-seconds after loops 2-6 and then serially for up to 15-minutes after loop 7. Nine

subjects demonstrated a ≥10% decrease from baseline in their FEV ₁(EIB+). Of the nine, five

showed significant drops after loop 1, and the other four significantly dropped between loops 2-7

with one EIB+ subject showing significant refractoriness. The authors concluded EIB occurs in

athletes during prolonged exercise with variable bronchial hyper-responsiveness onset that may

influence performance. The lack of significant refractoriness in their cohort is consistent with an

exercise bronchoconstrictive dysfunction and is different that asthma. This study’s lack of

support for airway refractoriness may have been due to the limited time 15-minutes for recovery

from exercise loop 1 to exercise loops 2-7 and the environmental exposure of the exercise.

The mechanism of EIB is in two primary theories, the osmotic theory (high VE rates

cause water loss in the airway) and the thermal theory (airway cooling and rewarming lead to

airway reactive hyperemia, edema, and obstruction). Either or both of these theories may

contribute to EIB (narrowing of the lower airway during and after exercise in the presence or

absence of clinically recognized asthma). The prevalence of EIB is common in 80-90% of

asthmatics, 12-19% of the general population and in elite athletes with severity, depending varies

based on the type of sport, the maximum exercise level, and certain environmental conditions

can vary up 24-60%. It is also suggested about 40-50% of the individuals with asthma may

exhibit a refractory period with a pre-exercise warm-up. In contrast, Rundell et al. (2003) suggest

EIB occurs in athletes (different from seen in asthmatics) during prolonged exercise with

variable bronchial hyper-responsiveness onset that may influence performance with only one of

nine elite cross-country skiers displaying significant refractoriness. The lack of support for

airway refractoriness may be influenced by limited time between the first trial (considered the

warm-up exercise) and the successive trials (15-minutes) and/or the environmental exposure.

EIB will be reviewed more fully in section III Respiratory System Warm-up.

1.6 Respiratory Muscle Training

Respiratory muscle training (RMT) can be divided into two distinctly different types,

which are respiratory muscle strength training (resistive or threshold) and endurance (hyperpnea)

training. These types have been used to improve the endurance performance of healthy, diseased,

and athletic individuals (Beckerman, Magadle, Weiner, & Weiner, 2005; Enright & Unnithan,

2011; Griffiths & McConnell, 2007; Hanel & Secher, 1991; Hostettler et al., 2012; Leddy et al.,

2007; Sonetti, Wetter, Pegelow, & Dempsey, 2001; Uemura, Lundgren, Ray, & Pendergast,

2012; Weiner, Azgad, Ganam, & Weiner, 1992). Most studies on RMT propose an enhancement

of endurance exercise performance in healthy and diseased individuals with less improvement

seen in highly fit individuals. The most common types, respiratory muscle strength training and

respiratory muscle endurance training, both have similar effect on performance improvements

(Hostettler et al., 2012). Respiratory muscle strength training is divided into two types of either

inspiratory and expiratory flow resistive-load or inspiratory and expiratory pressure threshold-

load training (A. K. McConnell & Romer, 2004). In the inspiratory and expiratory flow

resistive- load training model, individuals inspired or expired through a variable diameter orifice

device, and the smaller the orifice size the greater the work required for any giving constant flow

through the device. (Hostettler et al., 2012). In the inspiratory/expiratory pressure threshold-load

training model, individuals created negative pressure by breathing through a device while trying

to overcome a threshold-load set to initiate inspiration or expiration. Respiratory muscle

endurance training, also known as Voluntary Isocapnic Hyperpnea (VIH), requires individuals to

maintain high target levels of ventilation for a duration of up to 30-minutes (Coast et al., 1999;

A. K. McConnell & Romer, 2004). The involvement of high levels of hyperventilation for

prolonged periods with respiratory muscle endurance training makes the observed effect on the

inspiratory or expiratory muscles impossible to separate (A. McConnell, 2009). The combined

effect of inspiratory and expiratory muscle training is suggested to be superior in improving

performance (Hostettler et al., 2012). When using inspiratory and expiratory muscle training, it

is much easier to separate, thus giving a better indication of the role each muscle group has in

performance outcomes (A. McConnell, 2009). A study to examine any crossover trial effect

between inspiratory and expiratory muscle training found no significant effect of expiratory

muscle training on performance alone or coupled with inspiratory muscle training (Griffiths &

McConnell, 2007). It is also suggested that adding expiratory muscle training to inspiratory

muscle training during the same breath cycle may impair inspiratory muscle response to

inspiratory muscle training (A. McConnell, 2009).

Non-traditional Training Programs- Beckerman et al. (2005) set out to assess the long-

term effects of inspiratory muscle training on inspiratory muscle strength, exercise capacity,

perception of dyspnea, quality of life, and utilization of medical care in patients with COPD.

They evaluated 42 COPD patients with FEV ₁<50% of predicted (before and at 3, 6, 9, and 12

months during the training program) and randomly assigned them into either a training group

(21 subjects) who did inspiratory muscle training for 1 year or a control group (21 subjects) who

received training with very light load. The threshold intensity started at 15% of PImax for the first

week then progressed 5-10% daily until reaching 60%. This PImax value was maintained from

month one to month six of training. Subjects’ parameters assessed were the FVC, FEV₁, six-

minute walk test, PImax, perception of dyspnea, and health-related quality of life. The data

showed significant increases in inspiratory muscle strength (PImax) by the end of the third month

of training as well as an increase in the six-minute walk test. Significant improvement in quality

of life was seen at the end of the sixth month, and a significant decrease in perception of dyspnea

by the end of the ninth month was noted. All benefits were maintained throughout the 12-

months, and a decrease in health care usage was noted. The authors believe the data suggest the

long-term effect of inspiratory muscle training in COPD patients improved the measures of

exercise capacity, quality of life, and perception of dyspnea, as well as reduced health care

utilization. Other interesting observations were that none of the spirometry values significantly

changed over the duration of the study, and once a measure improved to a significant level,

there was very little additional improvement seen from continued increases in training

progression.

Weiner et al. (1992) examined adults with bronchial asthma by comparing specific

inspiratory muscle training and sham training (placebo) in on inspiratory muscle

strength/endurance, asthma symptoms, health care treatments for asthma, school or work missed

days, and medication use (inhaled β2-agonist). Thirty individuals with moderate to severe

asthma were divided into groups. One group of 15 individuals received the specific inspiratory

muscle training, and the other 15 individuals were assigned the control sham training. Both

groups trained five times a week for 30-minutes for six-month duration. The threshold intensity

started at 15% of PImax and progressed to 60% and then 80% for the last two months of training.

Results show significant increases in inspiratory muscle strength as evaluated by PImax at RV and

significant increases in respiratory muscle endurance as expressed by the relationship between

PmaxPeak and PImax in subjects in the specific inspiratory muscle-training group but not the sham-

training group. The specific inspiratory muscle-training group showed significant improvements

compared to the baseline data for asthma symptoms (nighttime asthma), morning tightness,

daytime asthma, and cough, inhaled β2-agonist usage, number of health care days or visits, and

amount of sick days missed due to asthma. The authors conclude a specific inspiratory muscle

training program for six-months improves respiratory muscle strength and endurance, as well as

in asthma related symptoms, health care usage, medication use, and loss work and school time.

The spirometry data from before and after training showed small but significant increases in

FVC and FEV ₁in the specific inspiratory muscle-training group as compared to the matched

control (sham) group. Five individuals were able to stop taking oral/IM corticosteroid

medications during specific inspiratory muscle training group as compared to only one in the

control sham group.

Hanel and Secher (1991) studied the effect of inspiratory muscle training for 10 minutes

twice a day for 27.5 days on ten subjects in the training group (about 50% of PImax intensity) and

ten subjects in a sham-training group. They obtained data pre- and post-training on maximal

oxygen uptake (VO2max) maximal ventilations, maximal breathing frequency during exercise, run

distance in 12-minutes on a track, resting PEF, FVC, FEV₁, PImax and alveolar oxygen tension

(pAO2). Results from the inspiratory muscle-training group showed a significantly increased

PImax, a slight but significant decrease in breathing frequency. All the other measures derived

from the inspiratory muscle-training group were similar to the control sham group. The author

suggest inspiratory muscle-training results in significant increased PImax but has no effect on

VO2max, run distance in 12-minutes, resting PEF, FVC, FEV₁, and alveolar oxygen tension

(pAO2). A possible limitation of this study was the training protocol parameters, which were

twice a day for 10-minutes and a total of 27.5 days and about 50% of PImax intensity as compared

to the previously reviewed study by Weiner et al. (1992). In this study, authors trained their

asthma patients five times a week for 30-minutes for a duration of six months at varying

intensities of up to 80% of PImax. Certainly, a comparison of a healthy subject’s respiratory

system to the respiratory system of an asthma patient’s is not same, but an increase in the

training protocol parameters (time, duration, and intensity) may have changed the results seen in

Hanel and Secher (1991) study.

Griffiths and McConnell (2006) investigated the effect of four weeks of inspiratory

muscle training and/or expiratory muscle training and the effect of a subsequent six-week trial of

combined inspiratory and expiratory muscle training in club-level oarsmen on rowing

performance. They studied seventeen male rowers before and after training with ten performing

inspiratory muscle training and seven performing expiratory muscle training. After the initial

four-weeks of the two training protocols (about 50% of PImax, and PEmax training intensity), all

subjects performed six-weeks of combined inspiratory and expiratory muscle training. The

measures evaluated at four and ten-weeks were PImax, PEmax, minute ventilation, max flow

volume loops (PIF, PEF, FVC, FEV ₁and FEF 50%) during an incremental rowing ergometer

step test and a six-minute all-out (6MAO) effort. Results show significant increases in PImax of

26%, an improvement in mean power during the (6MAO) of 2.7%, and a small decrease in heart

rate up to about 5% in the inspiratory muscle-training group. The expiratory muscle-training

group showed increased PEmax of 31% at the end of the intervention, but no other measure was

significant during the step test or the 6MOA test. The authors believe inspiratory muscle training

can improve rowing performance, but expiratory muscle training and a combination of

inspiratory and expiratory muscle training did not produce any significant change in

performance.

Enright and Unnithan (2011) evaluated the effect of inspiratory muscle training at

varying intensities on inspiratory muscle function, VC, TLC, work capacity, and power output

in forty healthy individuals. Subjects were randomly assigned to four groups. One group was

assigned to be control with no training. The other three groups completed an eight-week

inspiratory muscle-training program set at either 40, 60, or 80% of sustained PImax. Training was

done three days a week, with 24 hours separating training days. Before and after training

measures of body composition, VC, TLC, MIP, sustained MIP, work capacity and power output

were obtained. The results show significant increases in MIP and SMIP at all intensities (40, 60,

and 80%), whereas the 60 and 80% training intensities demonstrated increased significance in

work capacity and power output. The 80% training intensity was the only group to show

significant improvements in VC and TLC. The authors believe if substantial pressures are

generated during a program of high intensity inspiratory muscle training then significant

improvements in lung volumes, work capacity, and power output may be seen in healthy

subjects.

Uemura et al. (2012) compared two different types of respiratory muscle training on the

exercise performance of eight (four males and four females) experienced runners. The training

consisted of a four-week, twelve-session resistive respiratory muscle training (60% of PImax, and

PEmax intensity). Followed by a four-week, twelve-session VIH training (40% of the MVV/

breathing frequency) with the measures of spirometry (FVC, SVC, FEV₁, MVV PImax, PEmax,),

respiratory endurance time, VO2max, running time to voluntary exhaustion at 80% of VO2max,

blood lactate concentration, and minute ventilation obtained before and about five days after

each training protocol. Pre- and post-training changes were seen with resistive respiratory

muscle training improved inspiratory muscle strength significantly by 23.8% and 18.7% at rest

and post exercise run test, respectively. VIH training significantly increased respiratory

endurance time to exhaustion by 237.8%, SVC by 3.43 %, and decreased MVV by 20%. Both

respiratory training protocols significantly increased the duration of the endurance run by 17.7%

for the resistive respiratory muscle training and 45.5% for the VIH training. No other measures

showed significant change in either of the respiratory training protocols. Interesting to note was

after VIH training, FVC and FEV ₁did show slight increases, though not viewed as significant

by the authors. Also important to consider is comparing the two training protocols, VIH

followed inspiratory/expiratory muscle training, which may have an augmenting effect on the

VIH results.

Leddy et al. (2007) examined the effect of VIH training with the intensity set at about

50% of VC and MVV values for four-weeks and 30-minutes a day on the respiratory system and

running performance in twenty-two male competitive runners (fifteen in the training group and

seven in the control sham group). The measures assessed were FVC, FEV₁, MVV, MIP, MEP,

VO2max, four mile run-time, treadmill run-time to exhaustion at 80% of VO2max, serum lactate,

total ventilation, VO2, oxygen saturation, and cardiac output before and after the four-weeks

(post one day and post seven days) day of training. Spirometry data and four-mile run time

measured every month during the three-month maintenance period. The data show significant

improvements seven days post training in MVV (+10%), respiratory endurance (+208%),

treadmill run-time (+50%), along with reductions in four-mile run time (-4%), respiratory

breathing frequency (-6%), VE (-7%), VO2max (-6%), lactate (18%), during the treadmill run test.

Of these, the four-mile run time remained above pre-training levels for the three months

maintenance period where reduced VIH training was noted. The authors believe seven days of

rest following an intense four-week, VIH training program is important to reveal the ergogenic

effect gained by training and that the gain can be maintained during a subsequent period of

reduction in VIH training frequency.

Beckerman et al. (2005) and Weiner et al. (1992) researched the effect of inspiratory

muscle training on individuals with airway disease (COPD and Asthmatics) and found

improvements in exercise capacity, quality of life, asthma related symptoms, loss work and

school time, and perception of dyspnea, as well as reduced health care/medication utilization.

Four studies examined the effects of inspiratory or expiratory muscle training protocols. Hanel

and Secher (1991) showed significance only in PImax, but used a limited protocol in time,

duration, and intensity. In contrast, the remaining authors that utilized inspiratory muscle

training

protocols found significance in multiple measures, including increases in performance. Griffiths

and McConnell (2006) used six weeks of RMT training at 50% of PImax and PEmax, and found

inspiratory muscle training superior to expiratory muscle training in improving mean power

(2.7%) in a six-minute all-out rowing effort. Enright and Unnithan (2011) found performance

improvements (work capacity and power output) in their subjects at 60 and 80% of PImax training

intensity and three days a week for eight-weeks. Uemura et al. (2012) studied both

inspiratory/expiratory muscle training and VIH and found the VIH training to be superior in

enhancing performance (endurance run) over inspiratory/expiratory muscle training (45.5% and

17.7%, respectively), but both show increases. However, it should be noted that the four weeks

of VIH training followed the four-week inspiratory/expiratory muscle training, thus creating an

additive effect on the VIH results. Leddy et al. (2007) also examined an VIH training protocol

on running performance and found that treadmill run-time increased at day one post training

(29%) and seven days post-training (50%) in four-weeks of training for 30-minutes a day. Some

studies showed significance in pulmonary function measure with inspiratory muscle training

improvements in FVC and FEV₁ (Weiner et al., 1992) and VC and TLC at 80% intensity

training (Enright & Unnithan, 2011). Because of the nature of each training protocol, the

inspiratory or expiratory muscle training displayed significant improvements in PI max and PE max,

respectively (Griffiths & McConnell, 2007; Hanel & Secher, 1991; Uemura et al., 2012; Weiner

et al., 1992), and the VIH showed significance improvements in MVV (Leddy et al., 2007;

Uemura et al., 2012).

Traditional Training Programs- The beneficial effects of exercise are often seen in many

body systems with any type of exercise if performed on a consistent basis, across the life span of

all individuals. Exercise training can delay many pulmonary changes seen with ageing and

reduce other related risk factors to chronic lung disease, though many studies have been

inconsistent on the influence of exercise on pulmonary function (Huang & Osness, 2005).

Swimming and running are just two examples of aerobic exercise that can be considered the best

for maintaining health and physical fitness and are known to have a profound effect on lung

function for many individuals (Sable, Vaidya, & Sable, 2012). Research on the effect of

resistance training on pulmonary functions (Singh, Jani, John, Singh, & Joseley, 2011) is rare at

best, but the latest pulmonary rehabilitation guidelines recommend upper extremity resistance

training in COPD patients for improved reconditioning programs (Ries et al., 2007). The

following is a review of studies on the influence of general aerobic conditioning programs

(Sable et al., 2012; Shinde et al., 2013), the impact of high-intensity interval aerobic

conditioning programs on pulmonary functions (Dunham & Harms, 2012; Nourry, Deruelle,

Guinhouya, et al., 2005) and resistance training (Singh et al., 2011).

Sable et al. (2012) examined the pulmonary functions of two different groups of athletes,

swimmers and runners to make comparisons on lung function. Thirty swimmers who trained at

least two to three kilometers per day regularly were compared to a matched group of thirty

middle distance runners. Both groups trained for the previous three years. The measures of tidal

volume, FVC, FEV₁, and MVV were significantly higher in the swimming group than in the

running group. The authors believe the effect of swimming exercise influences lung volume

measurements because the respiratory muscles of swimmers are required to develop greater

pressure as a consequence of immersion in water during the respiratory cycle, leading to

functional improvements of the muscles (like the diaphragm) involved in breathing. This study

shed some light on the value of training the respiratory muscles through exercise as these

individuals trained for the last three years. It would be interesting to know the percentage

predicted values for each of the groups studied and how a control group of non-exercisers would

have changed the results.

Shinde et al. (2013) examined the effect of aerobic exercise training and yoga exercise on

weight reduction and pulmonary functions before and after exercise training (one-year). Sixty

male and female subjects (30-50 years) with diagnosed obesity (grade I or II as calculated via

BMI) were divided into two matched groups randomly. One group was the aerobic exercise

training group (walking, 45 to 60-minutes a day for five days a week) and the other as the yoga

exercise group (various yoga exercises, 45 to 60-minutes a day for five days a week). At the

one- year follow-up, the results showed significance improvements in the measures of BMI,

FVC, FEV₁/FVC, and MVV in the yoga group as compared to the aerobic training group. The

authors conclude regular practice of yoga is beneficial in weight reduction and improves

pulmonary functions. Certainly, one can view this research as very interesting, but the important

variable to keep in mind is that yoga emphasizes that use of breathing control and techniques

done in various postures/poses, which, in turn, may improve pulmonary function. In addition,

the aerobic exercise training group protocol did not control for exercise intensity, possibly the

cause of limited improvement.

Dunham and Harms (2012) set out to determine whether high-intensity interval training

(HIT) would increase respiratory muscle strength and expiratory flow rates more than aerobic

endurance training (ET) alone. Fifteen physically active healthy subjects were divided randomly

into either a high-intensity interval-training group (eight subjects) or an aerobic endurance-

training group (seven subjects). The high-intensity interval-training group completed a four-

week training program of three days a week, exercising on a cycle ergometer at 90% of VO2max

in intervals of one minute 90% work rate, then a three minute at 20-watts, and repeated the

interval for a total of 20-minutes. The endurance-training group completed the same four-weeks

of training, the same three days a week, but trained for 45-minutes at 60-70% of VO2max of

constant load cycling. Of the values assessed before, at two-weeks of training, and after the

completed training program, both groups showed significant improvements in VO2max (about 8-

10%), five mile time trial (6.5%) HIT and (4.4%) ET. Both groups significantly increased PImax

post training (43%) HIT and (25%) ET. The HIT group had significantly higher measures than

the ET group. No changes were noted in the expiratory flow rates in either training group. The

authors believe both whole-body aerobic endurance exercise training and high-intensity interval

training are effective in increasing inspiratory muscle strength, with HIT offering a more time-

efficient method than ET in improving aerobic capacity and performance. It is reasonable to

believe that the duration of the program (four-weeks) was the reason the training programs did

not have more of an effect to the pulmonary function values, but it should be noted that a closer

look at the PEF measure also demonstrated improvements (28% for HIT and 9% for ET) with

both training groups from pre-training values.

Nourry et al. (2005) investigated the effect of intermittent, short-duration, high-intensity

running training on resting and exercise pulmonary function in healthy, pre-pubescent children.

The training group consisted of three females and six males (age 9.7 years). They participated

in eight-weeks of high-intensity intermittent run training and compared to a control (regular

physical activities) group of four females and five males (age 10.3 years). The training group

performed their regular physical education in school and trained two additional days at a

percentage of their maximal aerobic speed (MAS, determined via a 20m shuttle run test). The

training sessions (about 30 minutes of total exercise) consisted of a warm-up of ten second runs

at 100% of MAS followed by a series of varying, four short, intermittent exercise runs (10-20

seconds runs at 100-130% range of MAS) separated by three minutes of passive recovery. After

the eight-week training program, no change was seen in the control group, but the training group

significantly increased FVC (7%), FEV ₁(11%), PEF (17%), FEF 50% (16%), FEF 75% (15%),

as well as, VO2max (15%), VE (16%), VT (15%). The author suggests eight-weeks of high-

intensity intermittent run training can improve resting pulmonary function and exercise

ventilation in prepubescent children.

Singh et al. (2011) examined the effect of upper-body resistance training on pulmonary

function in 30 male smokers (age 25-55 year). The subjects were randomly assigned to two

groups. One been an exercise group of fifteen subjects (experimental group, EG) and a second

non-exercise control group fifteen subjects (CG). The EG exercised for four-weeks, three times

a week on non-consecutive days, using upper-body resistance training (five major muscle

groups, 50-85% of the one rep maximum, three sets of ten repetitions) and conventional deep

breathing exercises. The CG only did conventional deep-breathing exercises and remained

inactive otherwise. Pulmonary function assessed before and after 4 weeks of training revealed

significant improvements FEV ₁(9%) and FEV₁/FVC (9%), but no change in FVC. The CG

groups had no significant changes noted, and removing any direct effect of the conventional

deep breathing exercises may have contributed to the improvements in pulmonary measures.

The authors concluded that four-weeks of upper-body resistance training program produced

significant changes in pulmonary functions in male sedentary smokers.

Sable et al. (2012) examined the pulmonary functions of two different groups of athletes,

swimmers and runners, and found swimmers displayed significantly higher pulmonary function

values than runners, the nature of which may be explained by the swimmers’ exposure to water

immersion increasing the pressure the respiratory muscles work against during their aerobic

training. Shinde et al. (2012) found the regular practice of yoga (> one year) as compared to

aerobic training is beneficial in weight reduction and improves pulmonary functions, which can

be attributed to use of breathing control, and techniques are done in various postures/poses

emphasized in yoga training. It is important to note that in the aerobic training group, the

training protocol did not control for intensity, thus limiting the results of this group. Dunham and

Harms (2012) used two training protocols (aerobic training and HIT) and found significant

improvements in performance (VO2max and time trials), as well as PI max, and PEF with both

training protocols, but the HIT group proved to be superior. Nourry et al. (2005) also

investigated an eight-week HIT program with significant improvements in performance (VO2max)

and pulmonary functions measures. Lastly, a study Singh et al. (2011) used upper body

resistance training to show improvements is pulmonary function measures in just four-weeks. As

shown here, regardless of the training traditional aerobic, yoga, HIT, or upper body resistance

training result in positive effects pulmonary function and enhanced performance. Something

interesting to note, is that of the protocols review here, the ones that challenged the respiratory

system (with high ventilation requirements or respiratory muscle work) produced the most

improvement.

1.7 Respiratory System Warm-up

This section will review that relevant research done on ways to use pre-exercise warm-up

to limit any EIB seen in individuals that may be prone to airway narrowing and any effects on

exercise performance. As discuss earlier, a refractory period may develop after specific warm-up

protocols, thus creating a period in which further vigorous exercise results in significantly less

severe or no EIB (Stickland et al., 2012). Refractory period may occur in about 40-50% of the

individuals that have an initial episode of EIB but then experience a diminished responsiveness

that can last from 1-4 hours after the initial warm-up exercise (Randolph, 1997). The mechanism

leading to a refractory period is unclear, but some suggest it may be mediated by a depletion of

catecholamine, an increase in circulation of prostaglandin, a degranulation of mast cells

mediators (Anderson & Holzer, 2000), or by an increase in bronchial blood flow and in the rate

of water return to the airway surface (Kippelen et al., 2012). The thought of a mechanism to

consistently create a refractory period in individuals with EIB or non-EIB individuals that

perform heavy intensity exercise that may be prone to EFL is very appealing because it could

promote fewer symptoms, decreased medication use, and improved exercise performance

(Stickland et al., 2012).

Research on the effects of pre-exercise warm-up can be divided into three areas based on

the type of warm-up protocol studied (interval, continuous high intensity, and continuous low

intensity). Some studies examined multiple types of warm-up strategies/protocols. Of the

interval type protocols, four studies will be reviewed (de Bisschop, Guenard, Desnot, &

Vergeret, 1999; McKenzie, McLuckie, & Stirling, 1994; Mickleborough, Lindley, & Turner,

2007; Zach, Schnall, & Landau, 1980); for the continuous high-intensity protocols, two studies

will be reviewed (Reiff, Choudry, Pride, & Ind, 1989; Zach et al., 1980); and for the continuous

low- intensity protocols, three studies with be reviewed (McKenzie et al., 1994; Morton, Fitch,

& Davis, 1979; Reiff et al., 1989).

The interval warm-up protocols involve repetitive sprints of 20-30 second duration at

100%+ of maximal effort (VO2max or higher) as a warm-up before an exercise challenge. Results

are compared to the same exercise challenge with no pre-challenge warm-up acting as the

control for the studies. The recovery time assessment of pulmonary function measures after the

exercise challenge varies up to ten minutes to intervals of 15, 25, and 80 minutes.

Research by de Bisschop et al. (1999) examined the effect of a warm-up protocol on

exercise-induced asthma in asthmatic children to allow them participate more fully in activities

that induce their asthma. In the first study, measurements of peak flows were assessed before,

during, and after (5 and 10 minute) a seven minute run (EX1) outdoors on a track in 16

asthmatic children (mean 11 years). Then three pre-EX2 warm-up schedules were used of

varying intensity/speed (SRWU 1=100%, SRWU 2=120%, and SRWU 3=130%) on different

days.

These SRWU consisted of a series of five short runs at a speed/intensity percentage of EX1 and

7.5% of the EX1 (distance achieved) with 1.5 minutes between runs and 5 minutes between two

series of runs and 10 minute recovery before EX2. In the second study, 30 young asthmatic

children (mean 12 years) performed a seven-minute run alone (EX1) or the same run (EX2) after

the SRWU2 schedule. In all trials, medication was withheld for 12 hours prior to testing. The

results showed that in 24 of 30 children, the fall in PEF after EX2 was significantly less than the

fall after EX1. The percentage fall in PEF after EX2 was significantly correlated to the same

changed induced by the SRWU2 protocol. From the SRWU2 protocol, the children were divided

into three sub groups: G1) increased PEF, 10 or 30 subjects, G2), 15% fall in PEF, 14 of 30

subjects, (G3). Fifteen percent fall in PEF 6 of 30 subjects. The G3 subgroups had no significant

change with the application of SRWU2 to EX2 recovery compared to EX1 recovery. The authors

believe the change in PEF after a SRWU period was a good predictor of the occurrence of

bronchoconstriction after EX2. Thus, a SRWU can reduce the decrease in PEF for most of the

children (24 or 30 subjects) in this study, thereby reducing subsequent post-exercise

bronchoconstriction. Subjects in G1 and G2 sub-groups also improved their distance by 5%

from EX1 to EX2, suggesting an enhancement in performance.

Mickleborough et al. (2007) investigated the efficacy of a high-intensity interval warm-

up protocol and compared it to medication dosing with salbutamol (commonly used β2- agonist

for prevention or relief of asthma symptoms) on the severity of EIB and whether a combination

of medication and a warm-up protocol provide greater protection against EIB that either

intervention alone. Eight moderately-trained recreational athletes with documented EIB were

tested in four experimental conditions: 1) control (CON); 2) an interval warm-up (WU)

consisting of 8x30 second runs at peak treadmill speed, with 45 seconds recovery between each

run; 3) inhaling 200µg of salbutamol (IH); and 4) combining both WU and IH treatments. The

four interventions were followed 15 minutes rest and then subjects performed an exercise

challenge test (85-90% of predicted maximal heart rate for eight minutes). Pulmonary functions

were measured before and after (1, 5, 10, 15 minutes recovery). Results reveled that in the CON

intervention the pre-to-post exercise mean drop FEV ₁in all eight subjects was -18.25%. The

mean decrease for the WU interventions post-exercise FEV ₁significantly reduced to only -9.1%

(falls below the diagnostic threshold of 10% decrease in FEV ₁post-exercise). The IH and

WU+IH interventions produced significant bronchodilation with mean maximum percentage

change of post-exercise FEV ₁following the IH was an increase of +8.9% and WU+IH +15.2%.

The FEF 25-75% also showed similar significance. The authors believe the data indicate that

repeated high intensity warm-up can lessen the EIB and that combining the WU and IH

interventions resulted in a substantial bronchodilation adding a protective effect against the

development of EIB as compared to the interventions alone.

McKensie et al. (1994) examined the protective effects of continuous low-intensity

warm-up and an interval warm-up exercise on post-exercise bronchoconstriction in athletes with

exercise-induced asthma. Twelve moderately trained subjects with asthma were tested under

three experimental conditions: 1) continuous warm-up (CW); 2) interval warm-up (IW); 3)

control (C). The CW intervention group performed 15 minutes of treadmill running at a velocity

of 60% of VO2max followed by two minute rest and then an exercise challenge test (ET=6

minutes at 90% VO2max). The IW intervention group preformed 8x30 second runs (1.5-minute

rest between each run) at intensity of 100% VO2max, followed by two-minute rest and then the

same ET. The C group only performed the ET. The measures of FVC, FEV ₁and mean

maximum PEF (MMPEF) were assessed (expressed as the percent change in baseline values) at

rest before any exercise condition and every 2 minutes during a 25 minute passive recovery

period. The results show significant difference in FEV₁, FVC, and MMPEF for the CW (16.7,

10.7, and 30.2

%, respectively) over the IW (29.7, 21.0, and 43.4 %, respectively) or the C (34.6, 30.0, and

50.0%, respectively). The author suggests a CW exercise of 15 minutes at 60% of VO2max can

significantly reduce post-exercise bronchoconstriction in moderately trained athletes with

asthma. The results suggest the CW protocol was significantly better than an IW protocol, but

the IW was still significantly better than the control. One could view the short rest period (2

minutes) between pre-exercise warm-ups as a limitation of this study possibly leading to the

limited results for interval warm-up as compared to the continuous warm-up.

Schnall et al. (1980) examined the notion of bronchodilation produced by short periods of

running in subjects in which EIB had occurred after a standard exercise test. Eight subjects (12-

31 years) with a previous history of EIB (free of symptoms of asthma who had received no

medication with in the last eight hour before testing) were tested on separate days with three test

trials. The trials were as follows: 1) running twice (run A and run B) on a treadmill (10% grade

and speed to produce a heart rate of 180b/m) for six-minutes each with a 49-minute break

between each run (control); 2) performed a six-minute running (run C) followed by ten-minute

rest then seven short runs (120-130% of the six-minute run) of 30 seconds each with rest periods

of 2.5 minutes between each short runs and then 20 minutes rest followed by a second period of

running for six-minutes (run D); and 3) performed seven-minutes of short runs was completed

20 minute before the six-minutes of running (run E). The data shows significant change in the

mean maximal post-exercise falls from baseline (resting) for the PEF, FEV₁, and FEF25-75%

measures comparing run A (control) 22.8, 23.0, and 37.3%, respectively, to run E (run following

short runs only) 10.4, 6.9, and 18.9%, respectively. The values (FEV ₁and PEF) for run D

revealed significantly less fall in the mean maximal post-exercise change in values that run A.

The authors suggest repeated, short runs minimize the bronchoconstricting effect on subsequent

exercise stress and have a bronchodilating effect on previous EIB. They also suggests the data

provide evidence to support that asthmatics cope better with repeated, short duration activities

and that warm-up period may be beneficial in alleviating the effects of more prolonged exercise.

The four studies outlined above using an interval protocol involved 52 subjects. The

protocols compared the percentage fall in FEV ₁and/or PEF on an exercise trial with and without

(control) an interval warm-up before. Spirometry measures after exercise trials were collected at

varying times (up 10, 15, 25, 80 minutes). The interval warm-up protocols consisted of repetitive

sprints of 26-30 seconds at maximal intensities (≥100% VO2max). The mean difference in the

maximal percent fall in FEV ₁and PEF from the control exercise trial as compared to the

exercise warm-up trial, ranged from about 4.9-16.1% and 11.6-30%, respectively. The data

supports significant difference from control to interval warm-up protocols and a general benefit

of these types of protocols. The recovery times between warm-ups and exercise test varied from

2 minutes up to 20 minutes. Two studies reported a performance measure (distance or VO2max)

during their studies; with de Bisschop et al. (1999) suggesting a 5% improvement in distance

cover on a track with interval warm-up and Mickleborough et al. (2007) reported no significant

improvement in VO2max with interval warm-up alone.

Continuous high-intensity protocols involve continuous high-intensity warm-up with a

control exercise challenge with no warm-up. The warm-up exercise intensity was on the high

end of VO2max (heart rate of 180 or 98% of max predicted) with the recovery pulmonary function

assessment measured up to 80-90 minutes after the exercise challenge.

Reiff et al. (1989) examined the effect of a prolonged warm-up period of exercise on

subjects with EIA. Seventeen asthmatic subjects with known EIA were tested using two different

randomized exercise protocols: 1) a 6-minute treadmill trial at 6 kph and 15% grade (S1A,

producing 98% of max predicted heart rate): (continuous high-intensity) followed by the same

exercise trial (S2A) with 45-minutes rest between (day A); 2) a 30-minute treadmill at 6 kph and

3% grade (W1B) with 21-minutes rest (continuous low-intensity warm-up) followed by the same

exercise test trial (S2B) used in day A (day B). The mean maximal percent fall in FEV ₁and PEF

from base line are as follows: S1A= 46% and 51%, respectively; S2A= 29% and 32%,

respectively; W1B= 17 % and 21%, respectively; S2B= 26% and 27%, respectively. The data

supporting refractoriness was demonstrated on the S2A compared to the S1A and that W1B

produced significantly less EIA than S1A with significant refractoriness to bronchoconstriction

after the S2B. The authors conclude a warm-up period of exercise can induce refractoriness to

EIA without itself producing marked bronchoconstriction.

Schnall et al. (1980), as review earlier, examined continuous high-intensity protocol vs.

interval warm-up protocols. The continuous high-intensity had subjects running twice (run A and

run B) on a treadmill (10% grade and speed to produce a heart rate of 180b/m) for six- minutes

each with a 49-minute rest between each run. The data suggest the interval warm-up protocol

was superior to continuous high-intensity protocol and had more significant change in the mean

maximal post-exercise falls from baseline (resting) than the use of run A (continuous high-

intensity warm-up) and then run B.

Continuous high-intensity protocols involve 25 subjects. The mean difference in fall from

baseline for FEV ₁and PEF ranged from 6.9-17% and 10.4-21%, respectively. The data supports

significant difference from control to continuous high-intensity protocols and suggests some

benefit of these types of protocols. The recovery times between warm-ups and exercise test were

from 20 or 49-minutes. None of the studies reported measures of performance.

Continuous low-intensity warm-up protocols use a warm-up exercise for duration of

three to 30 minute with an identical control challenge with no prior warm-up. The intensity for

these warm-up protocols used 60% of HRmax, 60% VO2max, or just a low intensity warm-up (30-

minute treadmill at 6 kph and 3% grade). The recovery pulmonary function assessments were

measured at up to 25, 30, and 90 minutes after the exercise challenge.

Morton et al. (1979) set out to determine the effect of warm-up on EIA. Eighteen subjects

(ten males and eight females) performed two trials of a five-minute sub-maximal treadmill

running to reach a heart rate of 85% of predicted maximum for age with one preceded by a

warm-up and one not preceded by a warm-up (control). The warm-up protocol involved walking

or jogging on a treadmill for three minutes to produce 60% of the subject’s maximum predicted

heart rate with less than a minute between completions of warm-up to the exercise test. The

results showed the mean maximal percentage fall in FEV ₁displayed no significant difference

from the two intervention trials (control and warm-up trials). The authors concede while their

study does not support the concept of warm-up to reduce the likelihood of EIA, the

recommendation of a longer, more intense warm-up involving interval activities should be

considered with future studies.

McKensie et al. (1994) as reviewed earlier compared a continuous warm-up (CW) and

interval warm-up (IW) exercise on post-exercise bronchoconstriction in athletes with exercise-

induced asthma (EIA). The subjects were tested under a CW protocol performing 15 minutes of

treadmill running at a velocity of 60% of VO2max followed by two-minute rest and then an

exercise challenge test (ET=6 minutes at 90% VO2max). The results suggest the CW protocol was

significantly better than an IW protocol but the IW was still significantly better than the control.

Reiff et al. (1989) as reviewed earlier, compared a continuous high-intensity warm-up

and a continuous low-intensity warm-up on subjects with EIA. The subjects were tested with a

continuous low-intensity warm-up protocol and performed a 30-minute treadmill at 6 kph and

3% grade warm-up with 21-minutes rest followed by the exercise test trial. The data suggest the

continuous low-intensity warm-up protocol produced significantly less EIA than the other

continuous high-intensity protocol.

The three studies using continuous low-intensity protocols involve 47 subjects. The mean

difference in fall from baseline for FEV ₁and PEF ranged from 16.7-29% and 30.2.-32%,

respectively. One study showed no significance in either measure (Morton et al., 1979). Most of

the data supports slight significant difference from control to continuous low-intensity protocols

and suggests some limited benefit of these types of protocols. The recovery times between

warm-ups and exercise test were from zero, 2, or 45-minutes. The zero-minute rest between

warm-up and exercise test protocol was also the study that showed no significance with a

continuous low-intensity. None of these studies reported measures of performance. Table1.1

summarizes these studies.

1.8 Implications for Future Research

Many physiological mechanisms have been proposed concerning why exercise may cause

airway refractoriness. The effect of exercise on the airway may result in dehydration of the

airway surface, leading to an increase in airway osmolarity. This increased osmolarity creates

inflammation, thereby releasing mediators of prostaglandins, leukotrienes, and histamine from

mast cells causing bronchoconstriction (Anderson & Holzer, 2000). Anderson and Holzer (2000)

noted that the mechanism of EIB in asthmatics may be of a different pathophysiological

mechanism than that of EIB in athletes. The causes of airway refractoriness are unclear, but it is

suggested that a depletion of catecholamines, an increased circulation of prostaglandin, or

degranulation of mast cells mediators are possible reasons. Regardless of the reasons, several

researchers have tried to develop studies that create refractoriness, thus improving pulmonary

functions in asthmatics and athletes alike. The thought of a mechanism to consistently create a

refractory period in individuals with EIB or non-EIB individuals that perform heavy intensity

exercise that may be prone to EFL is very appealing because it could promote fewer symptoms,

decreased medication use, and improved exercise performance (Stickland et al., 2012).

When examining the current and relevant research, one realizes that no single warm-up protocol

was consistently used in multiple studies. Though similar protocols may be grouped into general

categories, such as interval, continuous high-intensity, and continuous low-intensity, there

seems to be no agreement on the exact method to recommend. All the protocols reviewed use a

traditional training program (aerobic based or HIT based) for the basis of their warm-up

program. Five of the six studies that reviewed specific to warm-up protocols found significance

in pulmonary function measures as compared to controls. The one study (Morton et al., 1979)

with no significance in pulmonary function measures used a warm-up protocol that had no rest

Table 1.1 Summary of warm-up protocols.

Study Year Protocol

type(s)

Subjects/

Controls

Definition

of EIB %

fall in

FEV1

PFT Warm-up (WU) protocol Duration

WU and

(minutes)

Exercise

Test,

Time,

Type,

Intensity

% change of resting

FEV1 and/or (PEF)

de Bisschop 1999 Interval 36 (11-

years),

same

subjects

≥15%

FEV1

PEF 5 short runs at a

speed/intensity percentage of

EX1 (100, 120, or 130 %) and

7.5% of the EX1 (distance

achieved) with 1.5-minutes

between runs and 5-minutes

between 2 series of runs

10 7m

track@

max

effort

(26.8% over

controls of 37.9%

avg. for 3 groups)

McKenzie 1994 Interval & 12 (26.5 ≥15% FEV1 (continuous low-intensity) CW 2 6m TM CW=16.7%,

Continuous years), FEV1 performed 15-minutes of @ 90% IW=29.7%, and

Low-

Intensity

same

subjects

treadmill running at a velocity

of 60% of VO2max followed by

two-minute rest and then an

VO2max C=34.6%

(CW=30.2%,

IW=43.4%, and

exercise challenge test (ET=6 C=50%)

minutes at 90% VO2max).

(Interval) IW preformed 8x30

second runs (1.5-minute rest

between each run) at intensity

of 100% VO2max, followed by

two minute rest and then the

same ET.

Mickleborough 2007 Interval 8 (19.5 ≥10% FEV1, (Interval) warm-up (WU) 15 8m 9.1% over controls

years), FEV1 FVC, consisting of 8x30 seconds TM@ of 18.25%

same FEF runs at peak treadmill speed, 85-90%

subjects 25- with 45-seconds recovery MPHR

75% between each run

(Table 1.1 continued)

Schnall 1980 Interval & 6 (12-31 NR PEF, (control) & (continuous high- 49, 20 6m TM@ I=6.9% over

Continuous years), FEV1, intensity) running twice (run A 10% incl. controls of

Hi- same FEF 25- and run B) on a treadmill (10% HR=180 23.0%

Intensity subjects 75% grade and speed to produce a (I=10.4%

heart rate of 180b/m) for six- over 22.8%)

minutes each with a 49-minute IM=16%

break between each run (14%)

(Interval mixed) IM performed a

six-minute running (run C)

followed by ten minute rest then

seven short runs (120-130% of

the six minute run) of 30 second

each with rest periods of 2.5

minutes between each short runs

and then 20-minutes rest

followed by a second period of

running for six-minutes (run D)

(Interval) performed seven-

minutes of short runs was

completed 20-minute before the

six-minutes of running (run E).

Reiff 1989 Continuous 17 (16- ≥15% PEF, (control) & (continuous high- 45, 21 6m TM@ CL=17%

Hi- 32 FEV1 FEV1 intensity) a 6-minute treadmill 15% incl. over controls

Intensity & years), trial at 6 kph and 15% grade & 6km*h of 46%

Continuous same (S1A, producing 98% of max 97% 21% over

Low- subjects predicted heart rate) followed by MPHR 51%)

Intensity the same exercise trial (S2A) CH=29%

with 45-minutes rest between (32%)

(day A)

(continuous low-intensity) a 30-

minute treadmill at 6 kph and

3% grade (W1B) with 21-

minutes rest then followed by the

same exercise test trial (S2B)

used in day A (day B).

(Table 1.1 continued)

Morton 1979 Continuous 18 (11- ≥15% FEV1 a five-minute sub-maximal <1 5m TM @ No

Low- 33 FEV1 treadmill running to reach a heart 85% significance

Intensity years), rate of 85% of predicted MPHR

same maximum for age with one

subjects preceded by a warm-up and one

was not (control). The warm-up

protocol was walking or jogging

on a treadmill for three minutes

to produce 60% of the subject’s

maximum predicted heart rate

with less than a minute between

completions of warm-up to the

exercise test.

interval between warm-up exercise and the exercise test and possibly lead to the lack of airway

refractory observed. The one study (Morton et al., 1979) with no significance in pulmonary

function measures used a warm-up protocol that had no rest interval between warm-up exercise

and the exercise test and possibly lead to the lack of airway refractory observed. When

considering the effect of pre-exercise warm-up on performance measures, one study reported a

5% increase in distance with a high-intensity warm-up protocol (de Bisschop et al., 1999).

Questions remain as to what type of pre-exercise warm-up is best suited for the majority of

individuals that experience EIB or EFL and what effect on performance can be expected. Also of

interest is what other ways/modes may be used to improved measures with pre-exercise warm-

up.

As reviewed earlier, respiratory muscle fatigue can be a factor in the limitation and

development of EFL. Johnson et al. (1993) and Miller et al. (2006) suggest that even though the

diaphragm has substantial aerobic capacity, it will show significant fatigue during sustained

exhaustive exercise with intensities greater than 80-85% of VO2max. The force output required to

sustain VE during intense exercise requires significant muscle work (O2 demand) and a

significant proportion of the cardiac output to meet the applied intensity. It has been suggested

that the use of RMT or VIH (non-traditional traditional training programs) can enhance

endurance exercise performance in healthy and diseased individuals (Hostettler et al., 2012).

Singh et al. (2011) concluded that four-weeks of upper-body resistance training (traditional

resistance training program) produced significant changes in pulmonary functions in male

sedentary smokers. Thus, it would seem promising that the concept of warm-up for the

respiratory muscles directly would have some merit. Throughout this review process, this author

has had no knowledge of a study that has used non-traditional traditional or traditional resistance

training methods as a pre-exercise warm-up to directly warm-up the diaphragm and the

accessory muscles.

Finally, a number of limitations need to be considered. First, are respiratory muscle

fatigue and subsequent EFL avoidable with pre-exercise warm-up? Of the research on respiratory

muscle fatigue and EFL reviewed, all involved the measure of respiratory muscle fatigue and

EFL, and no study, to this author’s knowledge, examined the use of pre-exercise warm-up to

limit either. Second, is airway refractoriness a universal finding across individuals with and

without asthma? Of the pre-exercise warm-up research, all studied individuals with some degree

of asthma. It would be important to determine any effects on airway refractoriness in non-

asthmatics with pre-exercise warm-up. Third, does the use of pre-exercise warm-up enhance

performance? Reviewing the pre-exercise warm-up research, only two studies (of the six

reviewed) attempted measured performance outcomes. Only the study by de Bisschop et al.

(1999) demonstrated an increase in performance with pre-exercise warm-up. Thus, more

research should focus on how exercise performance may be enhanced with the use of pre-

exercise warm-up. Lastly, are there other modalities that can be used to enhance the outcomes of

pre-exercise warm-up? Of the reviewed research, all pre-exercise warm-up protocols included

traditional training types of activities. Could a pre-exercise warm-up using non-traditional

activities (RMT, VIH or upper-body resistance training) that are directly focus on the respiratory

muscles enhance pulmonary functions, but more importantly exercise performance?

Considering these areas of limitation in the reviewed research, what are the practical

implications for athletes and asthmatics? As demonstrated, a pre-exercise warm-up protocol

using traditional training methods showed improvement pulmonary functions in various groups

of asthmatics subjects. What if this improvement could be extended to athletes that compete in

multiple events with little rest recovery in between those events? Can the duration of recovery

be reduced with pre-exercise warm-up using traditional and/or non-traditional activities? Could

multi-event athletes see an improvement in subsequent event performances?

In conclusion, in an effort to find more efficient ways to enhance exercise performance,

this author believes an area that has shown merit is the use of a pre-exercise warm-up protocol.

More specifically, the use of traditional protocols (aerobic type and HIT) combined with non-

traditional protocols (RMT, VIH, and resistance training) may be the key to improved

performance for athletes and asthmatics alike. Future research along these lines should be

considered.

CHAPTER 2. EXPERIMENTS

2.1 Experiment 1

Introduction. Many authors have investigated respiratory system mechanics and its

limitation during exercise; likewise, respiratory muscle fatigue has been examined thoroughly by

measuring expiratory flow limitation (Babb, 2013; Bussotti et al., 2009; Guenette et al., 2007;

Swain, Rosenkranz, Beckman, & Harms, 2010), end expiratory lung volume (DeLorey, Wyrick,

& Babb, 2005; Guenette et al., 2007), exercise flow volume loops (Nourry, Deruelle, et al.,

2005b), work of breathing (Guenette et al., 2007), end inspiratory lung volume (Guenette et al.,

2007), maximal inspiratory pressure (Watsford, Murphy, & Pine, 2007), maximal expiratory

pressure (Watsford et al., 2007), and bilateral transcutaneous supra-maximal phrenic nerve

stimulation (Johnson et al., 1993). All of the above mentioned studies examined respiratory

muscle fatigue during exercise except for the bilateral transcutaneous supra-maximal phrenic

nerve stimulation study. The concept of respiratory system recovery after exercise has not

received empirical study, for example the time it takes the respiratory system to recover to

resting levels from maximal or near maximal exercise performance and the systems readiness for

another maximal or near maximal exercise performance.

With the lack of research in the area of respiratory recovery after exercise, the following

experiment was to examine the recovery of the respiratory system following exercise [as

measured by recovery flow volume loop (RFVL) and the return to a resting level (FVL)]. The

purpose of this study was to determine the effects of various exercise intensities on the measures

of pulmonary function (FVC, FEV1, FEF 25-75%, and PEF) during exercise recovery. The

hypothesis of this study was that following two-minutes of exercise on a bike ergometer at three

different intensity levels, (40, 65, and 90% of maximal predicted heart rate) the pulmonary

function will be significantly different at 0, 5, 10, and 20-minute post exercise recovery in young

healthy individuals.

Methods. Ten subjects on separate days at least 24-hours apart (five males and five

females) ages 18-32 (mean 22.6 years) performed two minutes of exercise at three different trial

intensities (40, 65, and 90% of maximal predicted heart rate) on an electronic braked cycle

ergometer (Ergometrics 800, Sensormedics). Subjects were instructed and self-reported that they

refrained from exercise, caffeine, and alcohol for 24-hours and had not eaten whole foods three

hours before testing. A 1.5-mile run for time was completed by the participants to estimate their

VO2max (George, Vehrs, Allsen, Fellingham, & Fisher, 1993; Larsen et al., 2002). Pulmonary

function via spirometry testing (FVC, FEV1, FEF 25-75%, and PEF) and cardiovascular [heart

rate, blood pressure, and blood oxygen saturation (SpO2)] data were measured before, during,

and after (0, 5, 10, and 20-minutes intervals) each exercise trial. The study was conducted in a

university-based kinesiology laboratory and the subject population of the study was drawn from

university student volunteers enrolled in Human Performance Education courses. Within the

study, volunteered subjects were excluded based on health status from the Physical Activity

Readiness Questionnaire (ParQ) (individuals with asthma, smokers, pregnant females, and others

that maybe at risk for exercise conditions were excluded). Volunteered subjects were informed of

the potential risks of the study and their written informed consent was given to participate prior

to beginning the study. This study was approved by the University’s Institutional Review Board

for use of human subjects (see Appendix).

Study Design. Subjects were randomly selected for trial conditions and completed an

informed consent form, a ParQ, a 1.5-mile run, and demographic assessments were collected

(height, weight, body compositions via bioelectrical impedance- Omron® HBF 306C, Omron,

Table 2.1.1: Demographics for Experiment 1.

Gender 5 males, 5 females

Age 22.6±9.4

Height inches 67.15±7.2

Weight pounds 153.8±66.2

Body Mass Index 23.673±7.2

Percentage of Body fat 17.98±12.9

Estimated VO2max 43.341±14.8

Corp., Schaumburg, IL) (Lukaski, Bolonchuk, Hall, & Siders, 1986) prior to spirometry testing.

Upon arriving for their testing, subjects were issued a single use Microgard® Disposable Filter

and performed resting spirometry followed by the randomized condition trial. Spirometry trials

were repeated as needed to achieve ATS standards for spirometry testing. Data from each

subject (spirometry, BP, HR, SpO2) was collected at each timed interval (0, 5, 10, and 20-

minutes).

Subsequent testing days followed with at least 24-hours in between trials. The subject’s heart

rate and SpO2 data was monitored by pulse oximetry (Nonin® 8600 pulse oximeter, Nonin

Medical Inc., Plymouth, MN). Once the resting spirometry data was collected, subjects assumed

the seated position (seat adjusted to approximately 30º of knee flexion) on the bike ergometer

and began pedaling to maintain a speed greater than 60 rpm for two-minutes. Pedaling

resistance was added to increase the subject’s HR to the required max predicted HR (40, 65, and

90% of maximal predicated heart rate) for at least the last 30-seconds of each bike trial.

Resistance was adjusted as needed to keep the subject’s HR and pedaling rpm in protocol

ranges. Once the bike trial was completed, the subject immediately sat down, donned provided

nose clips, and began the recovery spirometry testing. Recovery testing protocols were

completed after the 20-minutes of data collection interval.

Pulmonary Function Measurements. Spirometry measures were forced vital capacity

(FVC), forced expiratory volume in one second (FEV₁), forced expiratory flow 25-75% (FEF

25-75%), and peak expiratory flow (PEF). Sensormedics Vmax® 29c Pulmonary

Function/Cardiopulmonary Exercise Testing Instrument was used to collect the spirometry

values and the instrument (flow and volume sensor) was calibrated daily following American

Thoracic Society (ATS) accuracy standards (M. R. Miller et al., 2005). The laboratory

atmospheric ranges are as follows: 1) temperature 68-74° F, 2) 60-70% relative humidity, and 3)

barometric pressure 758-766 mmHg. Infection control was managed by instructing subjects to

wash hands upon entering the lab and each subject was assigned a sealed bag for their single use

Microgard® Disposable Filter. During all spirometry measurements, subjects were required to

sit with their noses clipped, and instructions were given by an experienced technician on the task

needed. All testing criteria followed ATS evaluation standards (M. R. Miller et al., 2005).

Data Analysis. With demographic data gathered prior to testing (age, gender), dependent

variables, such as included spirometry data (FVC, FEV₁, FEF 25-75%, and PEF),

anthropometric data (mass, stature body fatness and body mass index), and a timed 1.5-mile run

(predicted VO2) were utilized during the study. The independent variables were 40%, 65%, and

90% MPHR, and a timed post exercise (0, 5, 20, and 20-minutes). Following experimentation,

one-way repeated ANOVA measures were computed across the independent variables for each

respiratory measure and timed runs in order to determine if respiratory capacities had changed.

The criterion for statistical significance of the correlations was set at p ≤ 0.05. All statistical tests

were performed on SPSS version 21.0 (Chicago, IL, U.S.A.).

Results. Pulmonary capacities did not change significantly based on the intensity of the

exercise performed. There were no pulmonary function differences found at 0, 5, 10, or 20-

minute post exercise recovery times. The cardiovascular responses were normal.

Discussion. The purpose of this study was to determine the effects of various exercise

intensities (40, 65, and 90% of maximal predicated heart rate) on the measures of pulmonary

Table 2.1.2: ANOVA comparisons between conditions and time

Variable N Condition F Condition p Time F Time p

FVC 10 0.411 0.745 0.049 0.995

FEV1 10 1 0.393 1 0.409

FEF 25-75% 10 0.253 0.859 0.252 0.908

PEF 10 0.228 0.877 0.204 0.936

Note: Significance at p ≤ 0.05*

function (FVC, FEV1, FEF 25-75%, and PEF) during exercise recovery; and it was hypothesized

following two-minutes of exercise on a bike ergometer at three different intensities, (40, 65, and

90% of maximal predicated heart rate) the pulmonary function will be significantly different at

0, 5, 10, and 20-minute post-exercise recovery in young healthy individuals. The data suggests

there were no statistical difference between the pulmonary function measures at the various

exercise intensities tested.

Some possible areas of weakness of the study includes the limited sensitivity of

pulmonary function for the exercise intensities utilized and the exercise trial duration were not

extensive enough to cause changes in the respiratory system. Other sensitive methods may be

used to determine greater significance in distinguishing a change in an individual’s respiratory

system during exercise. Nourry et al. (2005) used maximal flow-volume loop (MFVL) at rest

and the exercise flow-volume loops (EFVL) (plotted in the MFVL) during a progressive exercise

test to exhaustion (eight to ten-minute duration). The results of the study showed higher FVC

and maximal expiratory flows in trained subjects’ verses untrained subjects’ thus suggesting that

EFVL may be a more sensitive method in seeing change in pulmonary function measures. Hill et

al. (1991) studied a group of triathletes to see what pulmonary function measures changed during

an endurance triathlon (long duration, multi-event). Pulmonary functions were obtained after

each event and 24 hours after the completed triathlon. Following the completion of the triathlon,

significant declines from baseline were noted in the FVC (7.1%), FEV ₁(8.4%), FEF 50% (18.6

%), FEF 25-75% (15.2%), but no change in MVV or the other FEF measures, ratio, and/or PEF

were demonstrated. These results suggest the duration (>12-hours) of the exercise is an

important variable reflective of declines in some pulmonary function measures. Though this

study illustrates long durations of exercise affecting pulmonary function of triathletes, it remains

to be determined at what timed interval the variables started to decline; it seems base on the

present studies protocols, it would be longer durations of greater than two-minutes.

There are limitations within this study, such as the control of intensity was difficult to

monitor because of the short duration of the activity protocol (two-minutes) and the adjustment

of intensity via manual resistance produced the heart rate to respond slower than the subjects’

fatigue. A longer duration of exercise time may have helped to control for this limitation and

allow a more comfortable ramping of the intensity. Secondly, the maximum (zero-minutes after

trial) recovery PFT was difficult to obtain for the 90% intensity protocol because most subjects

were breathing maximally and it was challenging to complete the PFT when subjects are

gasping for breath. An alternative to this limitation would have been to do a peak flow at the

maximum recovery and complete the first PFT at one minute of recovery. Lastly, the possibility

that the number of subjects in this study could weaken the statistical reliability can never be

discarded.

Conclusion. Exercise trials for two-minutes, at intensities of 40, 65, and 90% of their

maximum predicted heart rate, are not significantly taxing enough to produce changes in

pulmonary function measures in young healthy individuals. Though the data does not show

significant changes in pulmonary function measures with short durations of exercise with

varying intensity, the beneficial effects of such cannot be ruled out.

2.2 Experiment 2

Introduction. Many exercise physiologists believe the respiratory system has little to no

effect on limiting exercise performances in healthy individuals or athletes (A. McConnell,

2009), yet the respiratory system encounters several challenges during intense exercise. For

example, the regulation of alveolar partial pressure of oxygen and carbon dioxide is achieved by

a considerable increase in alveolar minute ventilation (VE) often 20-times the resting value in

humans. This large increase in VE is achieved by the capacity of the respiratory muscles to not

only generate forces to alveolar ventilation but also by limiting excessive physiological cost on

the system during exercise (Guenette & Sheel, 2007). An additional challenge the respiratory

system must overcome is the ability of the bronchial (intra-thoracic) airways to maintain patency

to allow the increase flow rate needed during active expiration often seen in intense exercise.

During high intensity exercise, the bronchial airways occasionally do present a significant

limitation to expiratory flow; thereby causing dynamic hyperinflation, increased respiratory

muscle work, and VE limitation (Forster et al., 2012).

Research on the value of pre-exercise warm-up has used only traditional training

protocols and methods [high intensity interval (HIT), continuous low intensity (CLI), and

continuous high intensity (CHI)] as the warm-up modes. Another possible way to reduce the

demand on the respiratory system’s muscles and change pulmonary function is the use of a pre-

exercise respiratory warm-up involving non-traditional training methods. Non-traditional

methods use respiratory muscle training devices (inspiratory and expiratory breathing methods)

to warm-up the respiratory muscles. Based on my literature review, no studies have used non-

traditional warm-up methods to warm-up before exercise performance, but some studies have

looked at the training effect of these types of training protocols (Griffiths & McConnell, 2007;

Singh et al., 2011; Weiner et al., 1992) on pulmonary functions.

Weiner et al. (1992) compared specific inspiratory muscle training versus sham (placebo)

training on inspiratory muscle strength and endurance in an adult bronchial asthma population.

The study observed increases in inspiratory muscle strength and endurance as well as increases

in the FVC (force vital capacity) and the FEV ₁(forced expiratory volume in one second) when

compared to the sham control group with six months of training. Griffiths and McConnell

(2006) investigated the effect of four-weeks of inspiratory muscle training and/or expiratory

muscle training and the subsequent effects of a six-week trial of combined inspiratory and

expiratory muscle training in club-level oarsmen on rowing performance. The results of the

study suggested an increase in inspiratory and expiratory muscle strength and improvements in

mean power rowing performance. Singh et al. (2011) examined the effect of upper-body

resistance training and conventional deep breathing exercises on pulmonary function in male

smokers. Results from the study indicated improvements in pulmonary functions (FEV ₁and

FEV₁/FVC). These studies suggest the use of non-traditional methods of training as an effective

way to improve pulmonary function, inspiratory and expiratory muscle strength, and exercise

performance.

The physiological and performance benefits demonstrated by the previous reviewed

studies of non-traditional methods of training are hypothesized to also benefit an individual’s

pulmonary functions and exercise performance when used as a pre-exercise warm-up. The aim of

this study was to determine which of the three conditions (inspiratory, expiratory, or combined)

produced the best and most intense warm-up as assessed by rating of perceived exertion (RPE)

for breathing, produced positive (increases) change in PF measures, and produced the most

favorable recovery interval for PF measures. Of the three warm-ups (i.e. IM, EM, and CM), it

was hypothesized the CM would stress the respiratory muscles to a greater degree (i.e. CM

would produce a higher RPE during the performance); and for all three warm-ups, respiratory

muscles will recover in ten-minutes (i.e. have the highest PF during recovery).

Methods. Ten male subjects (Table 2.2.1) aged 18 to 30 (mean 22.6 years) completed

each of the three warm-ups 24-hours apart. Subjects were instructed and self-reported that they

refrained from exercise, caffeine, and alcohol for 24-hours and had not eaten whole foods three

hours before testing. The study was conducted in a university-based kinesiology laboratory and

the subject population was drawn from university student volunteers (convenience sample).

Subject inclusion was only male subjects while exclusion was based on volunteers’ health status

from the Physical Activity Readiness Questionnaire (ParQ) (individuals with asthma, smokers,

and others that maybe at risk for exercise treatments were excluded). In addition, demographic

assessment (height, weight, body compositions via bioelectrical impedance- Omron® HBF

306C, Omron, Corp., Schaumburg, IL) (Lukaski et al., 1986) was completed prior to beginning

the study for use of standardizing subjects. The study was approved by the University’s

Institutional Review Board for use of human subjects (see Appendix).

Table 2.2.1: Demographics for Experiment 2.

Gender 10 males

Age 22.6±7.4

Height inches 68.2±5.2

Weight pounds 162.0±115.2

Body Mass Index 27.36±11.24

Percentage of Body fat 17.77±16.73

Study Design. Subjects practiced each randomly selected warm-up on separate days for a

duration of five-minutes (actual breathing) while seated with a nose clip on. After each one-

minute interval of the five-minute warm-up, subjects were asked to give a rating of perceived

exertion of breathing (RPE 1-10 point scale, Appendix 1.D.) and performed a peak flow (PF)

through a peak flow measuring device. Fifteen-second duration was allowed to complete the

RPE and PF measurement and then the warm-up continued. Each randomized warm-up was

performed for a total duration of six-minutes once the fifteen-seconds were added to assess the

RPE and PF at each one-minute interval. PF data were recorded up to ten minutes (1, 2, 3, 4, 5,

6, 8, and 10-minute intervals) following completion of warm-ups and was labeled as recovery.

Breathing Warm-ups. The three respiratory warm-ups/ treatments performed for this

study were: inspiratory (IM), expiratory (EM), and combined inspiratory and expiratory (CM)

conditions. For IM, subjects inhaled deeply and forcefully to inspiratory capacity (IC) at a rapid

flow on an incentive spirometer (IS) device that measured inspiratory volume while providing

visual feedback on high, medium, and low flow generated. Following inhalation, subjects were

asked to hold their breath for five-seconds, and then exhale slowly with a moderate force to

residual volume (RV). In EM, subjects were asked to inhale slowly to IC, hold their breath for

five-seconds and then exhaled forcefully at a rapid flow to RV through a Resistex® Mercury®

Resistance Exercisers (RM) device with variable expiratory resistive load setting [one to four

(minimum to maximum)]. The expiratory resistive load was on four for each subject. For CM,

subjects were asked to inhale deeply and forcefully to IC at a rapid flow on the IS device, hold

their breath for five-seconds, and then exhaled forcefully at a rapid flow through RM device to

RV. All warm-ups were practiced for five-minutes (actual breathing) in a seated position and

wearing nose clips.

Data Analysis. RPE and PF were the dependent variables in this study while the

independent variables were the warm-ups/treatments (IM, EM, and CM). Following

experimentation, paired sample t-tests were calculated to compare data from pre-warm-up to

during warm-up (Table 2.2.2). The criterion for statistical significance of the correlations was set

at p ≤ 0.05. All statistical tests were performed on SPSS version 21.0 (Chicago, IL, U.S.A.).

Results. As noted in Figure 2.2.1, CM produced an increase in PF after five-minutes of

the warm-up. In addition, CM resulted in a reasonably consistent pattern of increasing PF values.

The IC displayed a consistent decline throughout the warm-up period, but the EC had erratic

response up and down throughout. The data from the RPE during warm-ups are presented in

Figure 2.2.2. RPE displayed progressively increased throughout each warm-up with CM resulted

in the highest RPE value after five-minutes. The data in Figure 2.2.3 suggests the highest PF

values were achieved at four minutes of recovery for all warm-up conditions. PF decreased after

four minutes for all three warm-ups with CM remaining the highest at eight and ten minutes of

recovery. Overall, however, the pattern between warm-up procedures was the basically the same

for each procedure.

The paired sample t-test suggests there was a significant difference in the CM warm-up at

RPE4 (M=3.800, SD=1.398) and RPE5 (M=4.500, SD 1.509); t(9) =-3.280, p=0.010. No other

variable found statistically significance (Table 2.2.2).

Discussion. Although this is the first known study to investigate breathing warm-up

effects on RPE and PF, the aim of this study was to determine which of the three warm-ups (IM,

EM, or CM) produced the best and most intense warm-up as assessed by the rate of perceived

exertion (RPE) for breathing, producing positive (increases) change in PF measures. In addition,

the most favorable recovery interval is for determining how PF measures were investigated. It

was hypothesized that among the three warm-ups, CM would stress the respiratory muscles to a

greater degree (i.e. higher RPE during the performance) and regardless of the warm-up, the

respiratory muscles will recover in ten-minutes (i.e. highest PF observed during recovery).

0123456

Warm-up time intervals in minutes

Inspiratory

Expiratory

Combined

1.5

0.5

2.4

scale

3.4

32.

2.6

1-10 2.5

4.5

4.2

3.9

3.6

3.8

3.2

2.9

3.5

RPE

4.5

Average RPE during Warm-up over Time

Figure 2.2.1: Average PF during time interval for warm-ups.

Figure 2.2.2: Average RPE during warm-up time interval.

607

603

Warm-up time interval in minutes

604

Inspiratory

Expiratory

Combined

595

591

0123456

602

604604

611

613

L/sec. 610

605

600

595

590

585

615

619

618

624

634

640

635

630

625

620

615

Average PF during Warm-up over Time

Figure 2.2.3: Average recovery RPE time interval.

Table 2.2.2: T-test data for Peak Flow and RPE during warm-up: IM=Inspiratory,

EM=Expiratory and CM= Inspiratory/Expiratory

Condition N Mean Std. Deviation t df Sig. (2-tailed)

Peak Flow (PF)

IM Pre-PF 10 607.5000 73.68288 0.112 9 0.913

PF5 10 604.5000 117.05768

EM Pre-PF 10 616.5000 75.57373 1.342 9 0.212

PF5 10 595.5000 66.35134

CM Pre-PF 10 591.0000 81.16513 -1.637 9 0.136

PF5 10 624.5000 102.91447

Peak Flow (PF)

IM PF1 10 613.5000 79.16404 0.424 9 0.681

PF5 10 604.5000 117.05768

EM PF1 10 618.0000 73.15129 1.317 9 0.220

PF5 10 595.5000 66.35134

CM PF1 10 611.0000 89.00062 -0.566 9 0.585

PF5 10 624.5000 102.91447

Rating of Perceived Exertion Breathing (RPE)

IM RPE4 10 3.6000 1.34990 -1.964 9 0.081

RPE5 10 3.9000 1.59513

EM RPE4 10 4.0000 1.12472 -1.500 9 0.168

RPE5 10 4.2000 1.22927

CM RPE4 10 3.8000 1.39841 -3.280 9 0.010*

RPE5 10 4.5000 1.50923

Note: Significance at p ≤ 0.05*

Pre-PF= resting PF, PF1= PF at 1-minute of the treatment, PF5= PF at 5-minutes of the

treatment, RPE4= RPE at 4-minutes of the treatment, RPE5= RPE at 5-minutes of the treatment.

620

609

600

590

580

570

560

607 605

583

572

600

582

Inspiratory

Expiratory

Combined

0246810

Time intervals in minutes

617

610

593

618

L/sec. 610

630

631

625

620

639

637

650

641

631

660

650

640

630

Average Recovery PF over Time

The data in Figure 2.2.1 suggest the PF during the three warm-ups differed at the end of

five-minutes of treatment. The CM resulted in an increase in PF after five-minutes while

producing a reasonably consistent pattern of increasing PF values to the end of treatment. The

CM protocol required forced inhalation and exhalation on the breathing cycle thereby

emphasizing the use of inspiratory and expiratory muscles. IC and EC protocols only required

forced inhalations or exhalations, respectively, therefore emphasizing one side of the breathing

cycle. Because the CM utilized a two sided use of the respiratory muscles, it is believed that

work created greater airway flow than the other single sided respiratory movements (IC and

EC). Movements such as these increase the range of motion of the respiratory muscles allowing

for greater preparation of the respiratory system for subsequent forced inhaling and exhaling as

seen in the PF maneuver.

The information provided in Figure 2.2.2 is suggestive of RPE progressively increasing

throughout each warm-up with CM resulting in the highest RPE value after five minutes. The

paired sample t-test is supportive for this outcome suggesting an increase that is statistically

significance in the CM at RPE4 vs. RPE5. Since there is an effect in the CM forced inspiratory

and forced expiratory, an increased intensity is created across the breathing cycle. Even though

all warm-ups use the complete breathing cycle, the forced nature of the CM provides an

increased intensity. However, it should be noted real number differences between the warm-ups

RPE are small (3.9 IM, 4.2 EM, 4.5 CM).

The data from Figure 2.2.3 shows all warm-ups progressively increased PF values at one

minute of recovery up to a peak PF value at four minutes of recovery with PF values decreasing

afterwards. At the eight and ten minute timeframe of recovery, the PF of CM remained the

highest of the three warm-ups. These findings continue to suggest the two-sided force

involvement of the respiratory muscles in the CM warm-up allows the system to stay primed

longer.

Some limitations of this study include the calculations and comparisons were made with

in each of the warm-ups (i.e. CM, Pre-PF to CM PF5) and not across warm-ups (i.e. IM to CM).

Secondly, the use of PF maneuvers can display a large range of values based on the subjects’

effort as shown in figure 2.2.1. Thirdly, EC resulted in an inconsistent pattern related to poor

stability in subjects’ effort. More consistent coaching of the PF maneuver and repeat efforts for

the best value would help to alleviate these inconsistences. Lastly, the small sample size weakens

the statistical reliability.

Conclusion. For each of the three warm-ups, five-minutes appeared to be a sufficient

duration to benefit breathing without greatly challenging body systems (RPE of a proximally 4).

During CM, the PF increased from the start of the treatment and had a reasonable consistent

pattern after five-minutes. On the other hand, IM and EM decreased at the end of five-minutes.

In recovery, all conditions achieved their highest values at four-minutes and continually

decreased afterwards. Notwithstanding this decrease, CM remained the highest at ten-minutes of

recovery. Based on these findings, the CM appears to be the optimal breathing warm-up for the

experiments that follow.

2.3 Experiment 3

Introduction. Many exercise physiologists believe that the respiratory system has little to

no effect on limiting exercise performances in healthy individuals or athletes (A. McConnell,

2009), yet the respiratory system encounters several challenges during intense exercise. One

example is the regulation of alveolar partial pressure of oxygen and carbon dioxide is achieved

by a considerable increase in alveolar minute ventilation (VE) often 20-times the resting value in

humans. This large increase in VE is achieved by the capacity of the respiratory muscles to not

only generate forces to alveolar ventilation but also by limiting excessive physiological cost on

the system during exercise (Guenette & Sheel, 2007). Another example challenging the

respiratory system one must overcome is the ability of the bronchial (intra-thoracic) airways to

maintain patency in order to allow the increase flow rate needed during active expiration often

seen in intense exercise. During high intensity exercise, the bronchial airways, occasionally, do

present a significant limitation to expiratory flow; therefore, causing dynamic hyperinflation,

increased respiratory muscle work, and VE limitation (Forster et al., 2012).

An often-overlooked ingredient to a possible limitation of the respiratory system is how

the mechanical work of breathing has both sensory and metabolic repercussions. The perceived

work of breathing contributing to how hard the exercise feels (sensory) and the demands the

mechanical work of breathing places on the circulatory system for blood and oxygen to sustain

muscle contraction (metabolic) (A. McConnell, 2009). It has been suggested that the metabolic

and circulatory cost of a high mechanical work of breathing during maximal levels of VE can

amount to 8-10% of the VO2max (maximal oxygen consumption) and cardiac output in the

untrained individual and up to 14-16% of VO2max and cardiac output in highly-trained individuals

(Aaron et al., 1992; Harms, McClaran, et al., 1998). It is further noted, with research on blood

flow distribution, as the respiratory muscles are loaded, a reflex vasoconstriction is produced

resulting in decreased blood flow to the exercising limb. Conversely, when the respiratory

muscles were unloaded, a state of increased blood flow (dilation) existed in the exercising limb

muscles (Harms, Wetter, et al., 1998). This change in limb blood flow indicates a competitive

relationship between the muscles of locomotion and the muscles of respiration for limited

cardiac output (Guenette & Sheel, 2007). These findings may well represent the

respiratory system’s challenge to sustain airway patency in the face of maximal or near maximal

workloads, creating high VE demands, competition for the available cardiac output with limb

muscles, and variations in the respiratory muscles fatigue states.

Research on the value of pre-exercise warm-up has used only traditional training

protocols and methods [high intensity interval (HIT), continuous low intensity (CLI), and

continuous high intensity (CHI)] as the warm-up mode (McKenzie et al., 1994; Reiff et al., 1989;

Schnall & Landau, 1980). Reiff et al. (1989) examined the effect of a prolonged warm-up period

of exercise on subjects with exercise induced asthma (EIA) and found that both CLI and CHI

warm-ups suggest a benefit (protection from EIA) for their subjects. McKensie et al. (1994)

examined the protective effects of CLI warm-up and an interval warm-up (IW) exercise on post-

exercise bronchoconstriction in athletes with EIA and their findings suggest the CLI protocol

was significantly better than an IW protocol, but the IW was still significantly better than the

control group. Schnall et al. (1980) examined the notion of bronchodilation produced by short

periods of running (HIT) in subjects in which EIB had occurred after a standard exercise test.

Their findings are suggestive that the use of repeated, short runs minimize the EIB and had a

bronchodilating effect on previous EIB. Their research also suggest that the data provides

evidence to support asthmatics cope better with repeated, short duration activities (HIT) and a

warm-up period may be beneficial in alleviating the effects of more prolonged exercise.

These studies suggest the use of traditional training protocols as a pre-exercise warm-up

providing subjects with a positive change in their pulmonary function and reduced EIB.

Another possible way to reduce the demand on the respiratory system’s muscles and

change pulmonary function is the use of a pre-exercise respiratory warm-up that involves non-

traditional training methods. Non-traditional methods would use respiratory muscle training

devices (inspiratory and expiratory muscle methods) to warm-up the respiratory muscles. Based

on this author’s literature review, there are not any studies researched on non-traditional warm-

up methods to warm-up before exercise performance, but some studies have looked at the

training effect of these types of training protocols (Griffiths & McConnell, 2007; Singh et al.,

2011; Weiner et al., 1992) on pulmonary functions. Weiner et al. (1992) compared specific

inspiratory muscle training versus sham training on inspiratory muscle strength and endurance

in an adult bronchial asthma population. Observation of increases in inspiratory muscle strength

and endurance was found as well as increases in the FVC (force vital capacity) and the FEV ₁

(forced expiratory volume in one-second) when compared to the sham control group with six-

months of training. Griffiths and McConnell (2006) investigated the effect of four-weeks of

inspiratory muscle and/or expiratory muscle training and the subsequent effects of a six-week

trial of combined inspiratory and/or expiratory muscle training in club-level oarsmen on rowing

performance. The results of the study indicate an increase in inspiratory and expiratory muscle

strength along with improvements in mean power rowing performance. Singh et al. (2011)

examined the effect of upper-body resistance training and conventional deep breathing exercises

on pulmonary function in male smokers. The results indicated improvements in pulmonary

function (FEV ₁and FEV₁/FVC). These studies suggest the use of non-traditional methods of

training are an effective way to improve pulmonary function test, inspiratory and expiratory

muscle strength, and exercise performance.

Since traditional training methods used as a pre-exercise warm-up demonstrate positive

change in pulmonary function and performance, one may conclude a non-traditional method of

training used as pre-exercise warm-up may demonstrate similar benefits. The concept of non-

traditional methods used as a pre-exercise warm-up for the respiratory muscles to improve

pulmonary function and exercise performance is a novel idea and worthy of investigation. As

such, if a breathing warm-up can increase the mechanical advantage of the respiratory muscles

prior to exercise, subjects may reduce the oxygen and cardiac output requirements during the

initial stages for exercise. If oxygen consumption and cardiac output requirements of the

respiratory muscles can be reduced during the initial stages of exercise performances than one

might expect to appreciate a recovery benefit as well. Based on the results from experiment two

in this study, the combined inspiratory and expiratory breathing condition/warm-up (IEC from

here on) suggested better outcomes (most intense and increased PF) compared to either of the

other conditions inspiratory (IC) and expiratory (EC) studied alone. As such, this experiment is

an expanded examination of the IEC (warm-up) effect on performance, rating of perceived

exertional breathing, and pulmonary function. The aim of this study is to evaluate the impact of

a pre-exercise respiratory warm-up using non-traditional methods (combined inspiratory and

expiratory muscle training modalities) (IEC) on pulmonary function measures (FVC, FEV₁, FEF

25-75%, PF), performance time (300-yard shuttle and 1.5-mile run) and recovery rating of

perceived exertion (RPE) breathing. Thus, it is hypothesized the use of a pre-exercise respiratory

warm-up using non-traditional methods (combined inspiratory and expiratory muscle training

modalities) will increase pulmonary function measures (FVC, FEV₁, FEF 25-50%, PEF)

and increase performance (reduced time to completion) achieved in a 300-yard shuttle and the

1.5-mile run as compared to the control condition (CC) (no warm-up). A secondary hypothesis is

that fitness status of the subjects would not be related to decreases in performance time and

subjects would rate their perceived exertion of breathing (RPE 1-10 point scale, Appendix 1.D.)

level as lower during recovery from each run after the respiratory warm-up (IEC).

Methods. All twenty male subjects the study aged 20 to 34 (mean 24.3-years) completed

the four sessions of the study (Table 2.3.1). In addition, two subjects started the sessions but

were not able to complete the entire study because of scheduling conflicts; therefore, their data

was not incorporated into this experiment. The study was conducted in a university-based

kinesiology laboratory and gymnasium with the subject population was drawn from university

student volunteers (convenience sample). Subject inclusion was only male subjects while

exclusion was based on volunteers’ health status from the Physical Activity Readiness

Questionnaire (ParQ) (individuals with asthma, smokers, and others that maybe at risk for

exercise treatments were excluded). Subjects were informed of the potential risks and gave their

written informed consent to participate prior to beginning the study. This study was approved by

the University’s Institutional Review Board for use of human subjects (see Appendix).

After completion of the informed consent, ParQ, and baseline data (height, weight, body

fatness percent via bioelectrical impedance- Omron® HBF 306C, Omron, Corp., Schaumburg,

IL) (Lukaski et al., 1986) for standardizing subjects, all subjects performed an initial series of

resting PFT followed by a randomly assigned resting (no-warm-up) control condition (CC) for

five-minutes or respiratory warm-up for five-minutes using the IEC warm-up protocol. Subjects

were instructed to perform the respiratory warm-up as follows: 1) Inhale deeply and forcefully to

inspiratory capacity (IC) at a rapid flow on an incentive spirometer (IS device- measures

inspiratory volume while visually giving feedback on high, medium, and low flow generated); 2)

Hold the inhale (breath) for five-seconds; 3) Exhale forcefully at a rapid flow to residual volume

(RV) through the Resistex® Mercury® Resistance Exercisers (RM) device with variable

expiratory resistive load setting (set at 4 highest resistance) to RV. Once the five-minutes of CC

(no warm-up) or IEC (warm-up) was completed, subjects rested for five-minutes and then

performed a 300-yard shuttle run (50-yards each direction) (Cumming & Keynes, 1967) or a

1.5- mile run (running line for a consistent distance) (Larsen et al., 2002) for time in a

gymnasium [all subjects completed both the CC (no warm-up) and IEC (warm-up) on different

days for both runs]. Subjects were allowed limited self-directed stretching before runs. After

completion of the runs, subjects returned to the kinesiology lab for recovery testing starting with

PF and RPE for every minute for 15-minutes. At the 5, 10, and 15-minute intervals PFT data

was collected.

During each assessment interval subjects were seated and nose clipped. The test sequence

required four days (two days for CC and two days for IEC) for completion. All subjects

completed two 300-yard shuttle runs (one with warm-up, one without) and two 1.5-mile runs

(one with warm-up, one without). Subjects were instructed and self-reported that they refrained

from exercise, caffeine, and alcohol for 24-hours and had not eaten whole foods three hours

before testing. Testing sessions were 24-hours apart. Fitness status was determined by predicting

the subject’s VO2max from their best 1.5-mile run time (George et al., 1993; Larsen et al., 2002).

Table 2.3.1: Demographics for Experiment 3.

Gender 20 males

Age 24.2±9.8

Height inches 68.1±5.1

Weight pounds 163.5±76.5

Body Mass Index 24.6±16.2

Percentage of Body fat 11.7±10.9

Estimated VO2max 44.9±14.9

Pulmonary Function Measurements. Spirometry measures utilized were forced vital

capacity (FVC), forced expiratory volume in one second (FEV₁), forced expiratory flow 25-75%

(FEF 25-75%) and peak expiratory flow (PEF). All pulmonary measurements were made with a

Sensormedics Vmax® 29c Pulmonary Function/ Cardiopulmonary Exercise Testing Instrument.

The instrument’s (flow and volume sensor) were calibrated daily following American Thoracic

• Randomized Run (300 yard shuttle or 1.5 mile run).

• Every subject completed one no warm-up (CC) and one warm-up (IEC) 300

yard shuttle run.

• Every subject completed one no warm-up (CC) and one warm-up (IEC) 1.5 mile

run.

RPE/PF

PFT

Figure 2.3.1: Flow chart of subjects, interventions, and analysis.

• Subject screened (ParQ) and enrolled in study (n=22).

• 2 subjects unable to complete (schedule conflicts).

• Study subject total male (n=20).

• Informed consent.

• Initial Demographics (height, weight, BMI, body fatness, age, gender).

• Resting assessments: Initial PFT (FVC, FEV₁, FEF 25-75%, PEF), RPE, and

PF.

• Randomized seated condition for 5 minutes (CC=no warm-up, IEC= warm-up).

• Rest for 5 minutes both conditions.

• Immediate RPE for run upon completion.

• 1 minute RPE and PF (continued every minute to 15 minutes).

• Recovery PFT at 5, 10, and 15 minutes.

• Paired sample t-test of dependent variables (run performance time, RPE, FVC,

FEV₁, FEF 25-75%, and PEF to independent variables [conditions: no warm-up

(CC) v. warm-up (IEC)].

Society (ATS) accuracy standards (M. R. Miller et al., 2005). The laboratory atmospheric ranges

were as follows: 1) temperature 68-74° F, 2) 60-70% relative humidity, and 3) barometric

pressure 758-766 mmHg. Infection control was managed by instructing subjects to wash their

hands upon entering the lab and each subject was assigned a sealed bag for their assigned

Microgard® Disposable Filter that was used only by them for each spirometry test. During all

measurements, subjects were seated, their nose was clipped, and they were instructed on proper

testing technique by an experienced technician. All testing criteria followed the ATS evaluation

standards (M. R. Miller et al., 2005).

Data Analysis. The dependent variables included performance time, RPE, FVC, FEV₁,

FEF 25-75% and PEF and the independent variables are the conditions no warm-up (CC) and

warm-up (IEC). Following experimentation, paired sample t-tests were calculated to compare no

warm-up (CC) and warm-up (IEC) data. Additional, VO2max was plotted against percent of

improvement for run times. The criterion for statistical significance of the correlations was set at

p ≤ 0.05. All statistical tests were performed on SPSS version 21.0 (Chicago, IL, U.S.A.).

Results. There was a significant difference in the 300 yard shuttle run as shown in Figure

2.3.2 for the immediate post run RPE between no warm-up (CC) (M= 8.65, SD=0.587) and

warm-up (IEC)(M=9.1, SD=0.718); t(19)=-2.269, p=0.035, the two-minute recovery RPE no

warm-up (CC) (M=6.15, SD=1.268) and warm-up (IEC) (M= 6.8, SD=1.508); t(19)=-3.115,

p=0.006, and the seven-minute RPE no warm-up (CC) (M= 3.5, SD=1.235) and warm-up (IEC)

(M=4.05, SD=1.356); t(19)=-2.463, p=0.024. No other paired sample showed significance for

RPE recovery in the 300 yard shuttle run as well as in Figure 2.3.3 for the 1.5 mile run. Data in

Figure 2.3.4 suggest no relationship between VO2max and the percentage of improvement in

performance time for the 300-yard shuttle and 1.5-mile run.

1.5 Mile Run Average Recovery RPE vs. Time

No Warm-upWarm-up

RPE

1-106

scale

Run123456789101112131415

Recovery Time in minutes

Figure 2.3.2: Average recovery RPE for the 300-yard shuttle run comparing no warm-up (blue

bar) and warm-up (red bar) with standard deviations and significance at p ≤ 0.05*.

Figure 2.3.3: Average recovery RPE for the 1.5-mile run comparing no warm-up (blue bar)

and warm-up (red bar) with standard deviations and significance at p ≤ 0.05*.

Run123456789101112131415

Recovery Time in minutes

RPE

1-10

scale

Warm-upNo Warm-up

300 yard Shuttle Run Average Recovery RPE vs. Time

seconds 52

Time

Average Performance Time for 300 Yard Shuttle Run

No Warm-up

Warm-up

300 yd Shuttle Run

Figure 2.3.4: VO2max plotted with percent of improvement for the 300-yard shuttle and 1.5-mile

run performance times.

Comparisons in Figure 2.3.5 showed no significant difference for no warm-up (CC) and

warm-up (IEC) for subject’s performance time in the 300-yard shuttle (seconds); Conversely, in

Figure 2.3.6 for the 1.5-mile (minutes) run showed significance difference from no warm-up

(CC) (M= 13.108, SD=2.194) and warm-up (IEC) (M=12.683, SD=1.855); t(19)=2.160,

p=0.044

for subject’s performance time.

Figure 2.3.5: Average performance time for the 300 yard shuttle run comparing no warm-up

Relationship of % Improvement v. VO2max for 300-yard shuttle

run and 1.5-mile run

VO2max

ml/kg/min 30

Est. VO2max

-15-10-50510

% of Improvement

(blue bar) and warm-up (red bar) with standard deviations and significance at p ≤ 0.05*.

Figure 2.3.6: Average performance time for the 1.5-mile run comparing no warm-up (blue bar)

and warm-up (red bar) with standard deviations and significance at p ≤ 0.05*.

The recovery pulmonary function data for no warm-up (CC) compared to warm-up (IEC)

for 300-yard shuttle and 1.5-mile run, are presented in Figure 2.3.7 and 2.3.8, respectfully. There

was a significance difference for the FVC for no warm-up (CC) (M= 4.732, SD=0.626) and

warm-up (IEC) (M=4.607, SD=0.631); t(19)=3.197, p=0.005 and FEV ₁for no warm-up (CC)

(M= 3.960, SD=0.587) and warm-up (IEC) (M=3.860, SD=0.607); t(19)=3.050, p=0.007 for the

300 yard shuttle run at ten-minute interval (Figure 2.3.7) and in the FEV ₁for the 1.5-mile

(minutes) run for the no warm-up (CC) (M= 3.852, SD=0.556) and warm-up (IEC) (M=3.722,

SD=0.424); t(19)=2.160, p=0.017 at ten-minute recovery interval (Figure 2.3.8). No other paired

sample of pulmonary functions values demonstrated significance.

Discussion. This is the first known study to investigate the effects of a breathing warm-up

on recovery RPE breathing, run performance time, and recovery pulmonary function; therefore,

the aim of this study was to evaluate the effects of a breathing warm-up using a combined

inspiratory/expiratory (IEC) breathing warm-up on recovery rating of perceived exertion (RPE)

breathing, performance time (300-yard shuttle and 1.5-mile run), and pulmonary function

Average Performance Time for 1.5 Mile Run

Time

minutes No Warm-up

Warm-up

1.5 Mile Run

Average Recovery PFT values for 1.5 Mile Run

Volume6

No Warm-up 5m

Warm-up 5m

No Warm-up 10m

Warm-up 10m

No Warm-up 15m

Warm-up 15m

FVC (L) FEV₁ (L)FEF 25-75%PEF (L/s)

(L/s)

Figure 2.3.7: Average recovery PFT values for the 300 yard shuttle run comparing no warm-up

at 5-minute (light blue bar), at 10-minutes (gray bar), at 15-minutes (dark blue bar), and warm-

up at 5-minutes (orange bar), at 10-minutes (yellow bar), at 15-minutes (green bar), with

standard deviations and significance at p ≤ 0.05*.

Figure 2.3.8: Average recovery PFT values for the 1.5 mile run comparing no warm-up at 5-

minute (light blue bar), at 10-minutes (gray bar), at 15-minutes (dark blue bar), and warm-up

at 5-minutes (orange bar), at 10-minutes (yellow bar), at 15-minutes (green bar), with standard

deviations and significance at p ≤ 0.05*.

Average Recovery PFT values for 300 Yard Shuttle Run

Volume6**

No Warm-up 5m

Warm-up 5m

No Warm-up 10m

Warm-up 10m

No Warm-up 15m

Warm-up 15m

FVC (L) FEV₁ (L)FEF 25-75%PEF

(L/s)

measures (FVC, FEV₁, FEF 25-75%, and PEF). A secondary aim of this study was to determine

if the subjects’ performance improvement was affected by their fitness status (VO2max). The data

presented on run recovery RPE between no warm-up (CC) and warm-up (IEC) suggests there

was significant difference for the 300 yard shuttle run at the immediate post run RPE, the 2-

minute, and the 7-minute recovery RPE intervals and no significance differences demonstrated

for the 1.5 mile run recovery RPE for both conditions. The performance time in the 1.5-mile run

decreased by an average of 25 seconds (3.2% improvement) with warm-up (IEC) verses no

warm-up (CC). The significant difference suggested for the FVC and FEV ₁at the ten-minute

interval for 300-yard shuttle run and FEV ₁at the ten-minute interval for 1.5-mile run was not

consistent with the stated hypothesis; as it was believed the warm-up (IEC) would increase

pulmonary function. The remaining pulmonary function values lacked statistical significance.

This study suggests no relationships between VO2max and percentage improvement in the

performance time of both runs.

The data on run recovery RPE suggest there were some time intervals (immediate post

run, 2 and 7-minute) with significant differences between no warm-up (CC) and warm-up (IEC)

for the 300 yard shuttle run but not the 1.5 mile run. These differences suggest the warm-up

(IEC) actually increased the RPE in recovery. This outcome is possible because of the anaerobic

nature of the run (300-yard shuttle) taxing the respiratory system maximally for such a short

duration and compounded by the perception of the warm-up (IEC) just five-minutes earlier.

Furthermore, individuals without a known history of difficulty breathing, as seen in this

population of young healthy males, adjust to the metabolic demands such that they do not need

the benefits provided by the breathing warm-up used in this study (Forster & Pan, 1988). As

reviewed earlier, in healthy individuals, the dynamic capacity of the inspiratory and expiratory

muscles to force generate probably never limits the VE response to exercise (Guenette & Sheel,

2007), which is a reasonable explanation for lack of improvement seen across both runs (300-

yard shuttle and 1.5-mile) of this population.

This study suggested a significant 3.2% improvement in performance time in the 1.5-mile

run after the breathing warm-up (IEC). As indicated by de Bisschop et al. (1999) similar

improvements were seen after a traditional warm-up protocol from their research on asthmatic

children. Children improved their distance by 5% suggesting an enhancement in performance.

Anecdotal observations in this study, found subjects perceived breathing less at the start of the

1.5-mile run after the warm-up (IEC); however their recovery RPE was unchanged when

compared to the no warm-up (CC). How did these lower perceptions at the start of exercise

contribute to the performance improvements; and if so, by what means? Research on time to

exhaustion (performance) using loading and unloading of the respiratory muscles showed that

loading via resistive devices produced a decrease in time to exhaustion and unloading with a

PAV increased time to exhaustion averaging ±14-15% (Harms et al., 2000). These results

suggest that increased performance (time to exhaustion) effect may be explained with reduced

dyspnea perceptions secondary to reduced respiratory muscle work (Miller et al., 2006).

Logically, performing a warm-up of the respiratory system directly before an exercise

performance should reduce dyspnea perceptions, reduce respiratory muscle work, and produce

improvements in performance. One possible mechanism of this process can be explained as

priming the system as seen in traditional warm-up modalities reviewed earlier by many authors.

It was theorized that a breathing warm-up (IEC) would increase pulmonary function

compared to no warm-up (CC). The findings suggest a statistically significant decrease in the

FVC (2.7%) and FEV ₁(2.5%) at the ten-minute interval for the 300-yard shuttle run and FEV₁

(3.3%) at the ten-minute interval for 1.5-milerun for the warm-up. These results are similar to a

study produced by Coast et al. (1999) indicating the effects of a maximal exercise trial

(progressive maximal cycle ergometer test) in healthy subjects. A significant decrease in FVC

(7%) was observed immediately following the exercise trial. The authors suggest data indicates

pulmonary function and respiratory muscle strength may be altered following exercise; however,

it is important to note, the present study’s data should be viewed with caution as all significant

values are less than 130 ml which is considered within the standards of repeatability (≤150 ml)

for the FVC and FEV ₁measures (M. R. Miller et al., 2005).

In order to attempt to rule out fitness status (VO2max) as a limit to performance

improvements in this study, VO2max was plotted against performance time changes. The data

suggests a lack of a relationship between these variables.

In view of the limitations within this study, the following improvements should be

considered: The subject populations consisting of healthy young males with no previous

breathing challenges suggest a lack of significance improvement in perceived breathing for

conditions (CC and IEC) and both runs. Subsequently, these subjects’ perceptions of breathing

during rest, activity, and recovery may be less sensitive because they tend to recover rather

quickly from only having experienced breathing challenges during exercise at high intensity.

Secondly, the use of recovery PFT measures to determine statistical differences in apparently

healthy young males after exercise may not be sensitive enough to detect a direct effect of a

breathing warm-up. The use of breath by breath analysis to track trends in total respiratory rate

and tidal volumes during exercise; as well as exercise flow volume loops, may be a more precise

measuring tools. Conversely, the breathing challenge created by the change in respiratory system

structure (mouth piece, nose clips, and total mouth breathing) could possibly disguise any

positive change caused by the respiratory system warm-up. Lastly, the possibility that the

number of subjects in this study could weaken the statistical reliability can never be discarded.

The possibilities of future study would be to consider diverse populations of subjects,

those that have had breathing challenges before (asthmatics, chronic obstructive pulmonary

disease, the elderly, and congestive heart failure) which may benefit from the breathing warm-up

studied. The use more sensitive ways to measure the variables tested (breath by breath testing as

one possible tool). And lastly, attention should be given to an evaluation of the breathing warm-

up on more specific modalities (i.e. swimming, cycling, skiing, and/or 400 meter run) need to be

considered.

Conclusion. In the exploration of new ways to enhance performance during activities

where breathing may limit exercise, it was conceived that warming up the respiratory system

before exercise could indeed improve performance. Findings from this study demonstrated a

3.2% improvement in performance time in a 1.5-mile run incorporating the warm-up treatment.

Even though this improvement may not be viewed as a huge modification, when one considers

the approximate cost of breathing on the system up to 14-16% of VO2max and cardiac output in

highly-trained individuals (Aaron et al., 1992; Harms, McClaran, et al., 1998) it becomes clear

that any benefit can be appreciated. Miller et al. (2006) suggest that increase performances may

be explained with reduced dyspnea perceptions secondary to reduced respiratory muscle work.

The evidence presented in this study suggests a benefit to performing a warm-up of the

respiratory system directly before an exercise performance; the mechanism of which may be

explained by reduced dyspnea perceptions, reduced respiratory muscle work, thus producing

improvements in performance. A secondary mechanism can be explain by priming the

respiratory system as seen in traditional warm-up modalities priming the skeletal and circulatory

systems as reviewed earlier by many authors.

2.4 Experiment 4