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Dyspnea and Wheezing in the Athlete. Joel Shaw MAJ, MD Primary Care Sports Medicine March, 2007. Objectives. Definition Epidemiology Pathophysiology Presentation Diagnosis Treatment Differential Diagnosis. Mandatory Sports Medicine Cartoon. Definition.

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Dyspnea and Wheezing in the Athlete

Joel Shaw MAJ, MD

Primary Care Sports Medicine

March, 2007


  • Definition

  • Epidemiology

  • Pathophysiology

  • Presentation

  • Diagnosis

  • Treatment

  • Differential Diagnosis

Mandatory Sports Medicine Cartoon


  • Asthma- reversible airway obstruction caused by chronic airway inflammation and hyper-responsiveness.

  • Exercise-induced bronchospasm (EIB)- transient and reversible airway narrowing precipitated by vigorous exercise.


  • Chronic asthma

    • 1997 NIH expert panel on asthma

    • 17 million adults in US

    • 5 million children

EIB epidemiology

  • EIA affects 12-15% of college athletes

  • 80-90% of asthmatics report exercise as a trigger

  • EIA occurs in 80% of asthmatics who don’t use inhaled steroids and in 50% who do

  • 40% of allergic rhinitis/atopic dermratitis patients have EIA

  • 10% of normal subjects

Achievements by athletes

  • 1984 Los Angeles Summer Olympics

    • 67 of 597 US athletes had EIA (11.2%)

    • 41 of these athletes won medals

  • 1994 Nagano Winter Olympics

    • 17% of US Team had EIA

  • 1996 Atlanta Summer Olympics

    • 117 out of 699 US athletes had history of asthma and/or took medications (16.7%)

    • 35 of these athletes won medals

Olympic B-Agonist Use

  • Sydney 2000: >18% of athletes from Canada, US, GB, Australia, New Zealand

  • Sydney 2000: sports variation: triathlon 20%, cycling 17%, swimming 14.5%, track and field 4.1%

  • Nagono 1988: 14-20% in Norway, Sweden, US and Australia; 33% in Netherlands

Winter vs. Summer Olympics

42% elite cross country skiers Pohjantahti Scand J Med Sci Sports 2005.

50% of competitive ski mountaineers Durand Int J Sports Med 2005

EIB in Cross Country Skiers

Pathophysiology of EIBTheory #1

  • Thermal Hypothesis (cold air)

    • Airways are forced to warm large volumes of air during exercise

    • High ventilation rates and compensatory mouth breathing lead to airway cooling

    • Rapid airway rewarming post-exercise causes reactive hyperemia of the bronchial micro-vasculature and edema of the airway wall

Pathophysiology of EIB:Theory #2

  • Osmotic Hypothesis (water loss)

    • Airways are forced to humidify large volumes of dry air during exercise

    • High ventilation rates and compensatory mouth breathing lead to evaporative water loss

    • Airway dehydration causes increased surface osmolarity mast cell degranulation

      Chemical mediator release

      Bronchial smooth muscle contraction

      Increased bronchial blood flow/airway edema

Other theories for EIB

  • Dog model- airway remodeling similar to asthma after exposure to cold, dry air. Davis MSSE 2003

  • Sputum samples in EIB show increase in eosinophils. Kanazawa Chest 2002

  • Concentration of NO in sputum higher in EIB, which correlates with vascular permeability

  • Combination of vascular permeability, drying, inflammation, and airway remodeling

Clinical Effects of Cold Air

  • Swedish cross country skiers:

    33% incidence vs. 3% age-matched controls

  • Norwegian cross country skiers:

    14% compared to 5% age-matched controls

  • US winter sports athletes:

    23% incidence, 50% incidence for cross-country skiers

Evidence for chronic changes

  • Training >20 hours/week increased risk of asthma development.

  • Elite vs. lower level swimmer: 21 vs. 11.2%

  • Endobronchial biopsies cross country skiers: increased T-lymphocyte, macrophage, eosinophil, basement membrane tenascin expression (marker for airway modeling) vs. control

Poor correlation between self-reported symptoms and both lab and field challenge tests

61% of athletes who were positive on a field test reported symptoms

45% with a negative challenge reported symptoms

(Tikkanen et al. Med Sci Sports Exerc 1999)

Study of college athletes referred for PFT’s based on history consistent with EIA

Only 46% had a positive laboratory exercise challenge test

(Rice et al. Ann Allergy 1985)

Diagnosis of EIA/EIB based purely on symptoms may result in either over or underdiagnosis of the condition leading to the inappropriate use of medications

Presentation:Patient Symptom Accuracy

Making the Diagnosis:The Medical History

  • History of asthma or respiratory symptoms

    • Timing of the onset of symptoms

    • Duration and severity of symptoms

    • Triggers

    • ER visits/Hospitalizations/Intubations

  • History of allergic rhinitis or atopy

  • History of medication use or immunotherapy

  • Smoking history

  • Family history of asthma or atopy

Making the Diagnosis:The Medical History

  • Useful screening questions

    • Have you ever missed school or work due to chest tightness, coughing, wheezing, or prolonged shortness of breath?

    • Do you ever have chest tightness?

    • When you exercise, do you often have wheezing?

Clinical Presentation

  • Classic symptoms

    • Cough

    • Chest tightness

    • Shortness of breath

    • Burning chest pain

    • Wheezing is rare

  • Unrecognized symptoms

    • Excessive fatigue after exercise

    • Poor exercise tolerance

    • Decreased athletic performance

EIB symptoms

  • Most commonly symptomatic after exercise

    • 3 to 5 minutes after cessation of exercise

    • Peak 10 to 20 minutes after exercise

  • Late inflammatory phase

    • 2 to 12 hours after exercise

    • May persist for 1 or 2 days (URI?)

    • 30% of patients with EIB Lacroix Phys Sportmed 1999

Making the Diagnosis:Peak Expiratory Flow

  • PEF rate commonly reduced but cannot substitute for full PFT’s

    • Effort dependent

    • Less reproducible than FEV1

    • Portable devices varying between manufacturers

  • Ambulatory monitoring can help with the management of asthma

    • Look for asthma triggers

    • Empowers asthmatics to control their disease

    • Early signal for exacerbations

    • Monitor effectiveness of therapy

Making the Diagnosis:Spirometry

  • Measurement of the FEV1 is the best PFT for diagnosing asthma and assessing severity

  • Ensure consistent effort/reproducibility

  • Spirometry performed looking for baseline obstruction (FEV1/FVC <70%)

  • If obstruction perform bronchodilator response (BDR)

    • Look for 12% and 200mL improvement

Baseline PFT’s in mild asthmatics and

patients with EIB are usually normal

Making the DiagnosisBronchial Provocation Testing

  • After baseline PFT

  • Bronchial provocation testing (BPT) is essential to demonstrate objective evidence of airway hyperresponsiveness.

    • Methacholine Challenge

    • Exercise Challenge

    • Eucapnic Voluntary Hyperventilation

Making the DiagnosisMethacholine Challenge Test

  • More sensitive than exercise challenge

  • Low specificity at higher doses.

    • Other conditions can have a positive MC.

      • Allergic Rhinitis (~30%)

      • Vocal Cord Dysfunction

      • Chronic Bronchitis (~20%)

      • Smoking

  • 1999 ATS Guidelines:

    • When pretest likelihood of asthma is 30-70%.

      • Negative predictive power >90%

      • Positive predictive power 90-98% (at PC20 1mg/ml) and 70% (at PC20 4mg/ml).

Making the DiagnosisExercise Challenge

  • 8-10 minutes minimum of hard exercise without warm-up, following by serial spirometry post exercise

  • Reproduces environment more accurately

  • More sensitive than indoor treadmill tests

  • Lack of standardization in methods and interpretation of results

    • Positive test: >10% drop in FEV1

  • Requires access to spirometry to be accurate

    • PEF less reliable

  • Requires available trained personnel to administer

Making the DiagnosisEucapnic Voluntary Hyperventilation

  • Voluntary hyperventilation of dry air containing 5% carbon dioxide

    • Steady state protocol: 85% max ventilation for 6 minutes

  • Similar airway response to exercise at the same ventilation

  • High specificity for asthma

    • 100% with 20% drop of FEV1

  • Major problem is access to centers performing the test

EVH compared to Exercise

  • Similar level of ventilation and inhaled water content of the inspired air

  • Airway response on most occasions is delayed to after the test

  • Majority of subjects have maximum airway response within 10 minutes of cessation

  • Increasing duration of challenge increases the response

  • Respond to same drugs

  • Production of refractory period

Environmental Control:Allergen and Irritant Avoidance

  • Dander and Dust mite control

    • Mattress covers

    • Frequent cleaning

    • Avoid carpets

  • Choose pets wisely

  • Avoid outside activities during peak exposures

    • High pollen counts

    • Smog/Ozone alerts

Environmental Control:Sport Selection for Asthmatics

  • Choose warm, humid environment over cold and dry

  • Choose short burst activities over prolonged steady exercise

  • Avoid asthma triggers especially for outside activities

Environmental Control:Sport Selection for Asthmatics

  • Avoid highly asthmogenic activities

    • High minute ventilation

      • Distance running

      • Cycling

      • Soccer

      • Basketball

      • Rugby

    • Cool & dry climate

      • Ice hockey/ skating, Cross-country skiing

Environmental Control:Sport Selection for Asthmatics

  • Good Choices:

    • Swimming/Diving

    • Gymnastics

    • Sprints/Field Events

    • Volleyball

    • Baseball

    • Tennis

    • Golf

    • Goal Keeper

Use of a mask

Capture heat and water on expiration

Found successful in reducing severity of EIA

Would you wear one??

Nose breathing

Promotes inhalation of humidified air

Achieves similar effect as mask

Natural switch to mouth breathing at 35 L/min

Buteyko Breathing Technique

Developed in 1960’s—to avoid hyperventilation and restore CO2 levels to normal

Involves controlled shallow breathing with intermittent breath holding

Popular in Australia and New Zealand

Warm-up/Refractory Period

30 second sprints vs. continuous low-intensity warm-up

Shown to induce 1-2 hour refractory period

May be due to improved bronchial blood flow and H2O delivery to surface

Only effective in approximately 50% of asthmatics

Inhibited by NSAIDs

Behavioral Control:Sport Performance for Asthmatics

Asthma exacerbation treatment

  • Baseline Peak Expiratory Flow (PEF)

  • Albuterol- 2 puffs now

  • Oxygen if available and needed

  • Ambulance vs. watch.

Return to play

  • Peak expiratory flow

    • Green- >80%

      • May compete with observation

    • Yellow- 50-80%

      • Treat and watch

    • Red- <50%

      • Transfer

Medical Treatment For AsthmaBeta2-Agonists

  • The most effective drugs for acute symptom relief

  • Mechanism

    • Relax bronchial smooth musclebronchodilation

    • Prevent mediator release from mast cells

    • Modify contractile effect of mediators on smooth muscle

  • Short-acting agents used as first line agents for pre-treatment prior to exercise in recreational athletes and those performing intermittent exercise

Medical Treatment For AsthmaBeta2-Agonists

  • Short-acting agents—2 puffs 15-30 minutes prior to activity – lasts 2-4 hours

    • Albuterol (Proventil)

    • Terbutaline (Brethaire)

    • Pirbuterol (Maxair)

    • Bitolterol (Tornalate)

  • Long-acting agents—2 puffs 30-60 minutes prior to activity – lasts 8-12 hours

    • Salmeterol (Serevent)

    • Formoterol—immediate and long acting

Medical Treatment For AsthmaBeta2-Agonists: Problems

  • Tolerance develops with prolonged, regular use of Beta-Agonists

    • Poor asthma control

    • Increased bronchial hyperresponsiveness

    • May result in reduction in baseline lung function if underlying inflammation not controlled in chronic asthmatic

  • Not recommended for prevention of EIA in regular exercisers with frequent symptoms or elite athletes

Medical Treatment For AsthmaMast Cell Stabilizers

  • Stabilize mast cell basement membrane preventing degranulation

  • Effective in early and late phase reaction

  • No bronchodilator effect

  • Sodium cromoglycate (Intal)

    • 2 puffs 30 minutes prior to exercise

    • Lasts 2 hours

  • Nedocromil sodium (Tilade)

    • 2 puffs 30 minutes prior to exercise

    • Lasts up to 4 hours

Medical Treatment For AsthmaAcetylcholine Receptor Antagonist

  • Ipratropium (Atrovent)

    • Short-acting bronchodilator with duration of 3-5 hours

    • 2 puffs 15 minutes prior to exercise

  • Individual response varies

  • Useful as alternate to or in combination with albuterol or mast cell stabilizer

  • Consider for:

    • Beta-agonist intolerance

    • Incomplete relief with beta-agonist or mast cell stabilizer

Leukotrienes are potent inflammatory mediators


Increase mucus production

Increase vascular permeability leading to airway edema

LTI’s block action of leukotrienes at the CysLT1 receptor

Montelukast (Singulair) 10mg once daily

Zafirlukast (Accolate) 20mg twice daily

Daily treatment is effective in preventing EIA/EIB

Studies show an immediate decreased inflammatory and bronchoconstrictor response when given prior to exercise Rundell Br J Sports Med 2005

Long term they are more effective than salmeterol

No tolerance is observed

Medical Treatment For AsthmaLeukotriene Receptor Inhibitors

Medical Treatment For AsthmaOther Agents

  • Non-sedating anti-histamines

    • Consider in patients with allergic rhinitis or allergic triggers

  • Immunotherapy

    • For atopic patients not otherwise controlled or intolerant of meds

    • Base on skin test results

  • Caffeine

    • Bronchodilator and reduces respiratory muscle fatigue

First line therapy for chronic asthma

Also consider in elite athletes who train nearly daily and require consistent prophylaxis

Alleviate post-exercise cough

Frequent late phase symptoms

Inhaled Corticosteroids

Triamcinolone (Azmacort)

Flunisolide (AeroBid)

Fluticasone (Flovent)


Medical Treatment For AsthmaInhaled Steroids

New research

  • 2 grams Vitamin C 1 hour before exercise- 9/20 patients responded Cohen in Arch Ped Adol Med

  • Once daily treatment with Singulair at bedtime blocked 47% fall in FEV1NEJM July 98

  • Omega 3 Polyunsaturated fatty acids (fish oil supplementation) blocked 80% of fall in FEV1Mickleborough Am J Resp Crit Care Med 2003

  • Inhaled heparin blocked 78% of drop when used 1 hour before exercise

Mild Intermittent

Beta2 agonist or mast cell stabilizer as needed

Mild Persistent

Inhaled low-potency corticosteroid

Short-acting Beta-agonist as needed

+/- long acting Beta agonist or leukotriene inhibitor

Moderate Persistent

Inhaled medium-potency corticosteroid

Long-acting beta agonist

Leukotriene inhibitor

Short-acting Beta-agonist as needed

Severe Persistent

As above but increase to high-potency steroid

Medical Treatment For AsthmaStepwise Approach

Consider immunotherapy if atopic

EIB Treatment Algorithm















Add daily medications step-wise



Maximize medications

Evaluate for other conditions

Bronchoprovocation testing

Concerns Unique to the Athlete

  • Most studies indicate increase in muscle strength and endurance in non-asthmatics who use Beta-Agonists

  • Salbutamol increased strength in 16 of 16 and endurance in 10 of 16 non-asthmatic men tested Van Baak MSSE 2000

  • Athletes believe it is ergogenic

  • IOC ban suggests experts believe the same

USOC Permitted




USOC Prohibited




Oral, rectal, IM or IV corticosteroids

Oral or injected Beta-agonists

USOC notification required and by inhalation only












Concerns Unique to the AthleteControlled Medications and Anti-Doping

Concerns Unique to the AthleteControlled Medications and Anti-Doping

  • September 2001 IOC Anti-Doping Code Update

    • Written notification by a respiratory or team physician to the relevant medical authority 1 week prior to competition including:

      • Detailed report of symptoms

      • Hospital/Clinic medical records

      • Evidence of positive bronchodilator test, positive exercise challenge test or a positive methacholine challenge test

  • At the Olympics, athletes who request use of inhaled Beta-Agonists will be accessed by an independent medical panel

  • Questionable cases will be retested prior to Games

EIB Testing in the 2002 Winter Olympics

  • 135 of 147 EIB challenge tests were approved

  • FEV1 response to bronchodilators averaged 16.2%

  • ECT led to 15.9% average drop in FEV1

Controlled Medications and Anti-Doping

  • Medication information and documentation requirements

  • World Anti-Doping Agency (WADA)

    • www.wada-ama.org

  • United States Anti Doping Agency (USADA)

    • www.usantidoping.org

Differential Diagnosis

  • All that wheezes is not asthma.

  • Asthma doesn’t always wheeze.

Differential Diagnosis

  • Vocal cord dysfunction

  • Gastroesophageal reflux disease

  • Chronic inflammatory asthma-like condition

  • Laryngopharungeal reflux

Vocal Cord Dysfunction- Prevalence

  • 10-15% of unresponsive asthma

  • Correlation with psychiatric disorder

  • Female:male > 2:1

  • Age: 20-40 yoa

Vocal cord closing

Normal- during inspiration

VCD- during expiration



Exposure (smoke, chemicals, pollution)



Cold air


Vocal Cord Dysfunction- Pathogenesis

Vocal Cord Dysfunction- Symptoms

  • Dyspnea

  • Wheeze

  • Cough

  • Chest tightness

Vocal Cord Dysfunction- Physical Exam

  • Normal at rest

  • Stridor

    • During or after exercise

      • Often early in exercise

    • During stressful situations

Vocal Cord Dysfunction- Diagnosis

  • PFT’s

    • Flattening of inspiratory loop

    • Only positive if performed while symptomatic

  • Direct Laryngoscopy

    • Gold standard

    • Performed when patient is symptomatic

Vocal Cord Dysfunction- Treatment

  • Classic asthma medications

    • Usually no change unless combined disorder

  • Breathing exercises

    • Abdominal breathingrelax upper respiratory musculature

  • Stress management

  • Medications

    • Heliox (20-40% helium in O2)

    • Botulinum toxin injection


  • Common in asthmatic patients

    • 199 asthmatic patients: 82% reflux symptoms, 72% +esophageal pH testing Harding Chest 1999

    • Adults with asthma: 77% heartburn, 55% regurgitation, 24% dysphagia Field Chest 1996

    • Children with asthma: similar GERD rate to adults based on 24 hour esophageal pH testing Harding Am J Med 2003

GERD as trigger for asthma

  • Not proven

  • Proposed meachnisms

    • Aspiration/microaspiration in tracheobronchial tree

    • Acid-induced esophago-bronchial vagal reflexes mediated by receptors in esophageal wall

GERD and Asthma

  • #1- Stimulation of vagal afferents

    • Microaspiration

    • Acid refluxed directly onto esophageal epithelium

  • #2- Airway vagal efferent response

  • #3- Pulmonary neuroinflammatory changes

    • Airway edema

    • Mucus production

    • Inflammation

    • Bronchial smooth muscle constriction



Food type

Meal timing

Raise head of bed

Weight control

Stress management

Avoid tobacco products



Proton pump inhibitors

Treatment of GERD for Respiratory Symptoms

GERD treatment

  • Is GERD treatment beneficial for asthma

    • May improve subjective symptoms

    • May reduce medication requirements

    • No evidence of improved lung function by spirometry

GERD response to Albuterol

  • Effects of Albuterol

    • Reduction of LES tone

    • Reduction of esophageal contraction amplitude

Chronic Inflammatory Asthma-like Condition

  • Cold weather athletes

  • High ventilation rates under specific conditions

    • Cold, dry air

    • Exposure to volatized fluorocarbons (ski wax rooms)

    • Exposure to exhaust from ice resurfacing machines

Chronic Inflammatory Asthma-like Condition

  • Airway remodeling pathologically different from asthma

  • Similar symptoms to EIB

  • May not respond to Albuterol

    • EIB+ short-track speedskaters did not improve airway function with Albuterol Wilber Chest 2001

      • Inflammation not addressed (inhaled steroids)

      • Consider in-rink testing

Laryngopharyngeal reflux

  • Prevalence

    • Unknown

  • Pathogenesis

    • Reflux reaches the UES causing irritation of the larynx and pharynx

    • Small amounts of acid exposure can cause significant irritation

Laryngopharyngeal Reflux- Symptoms

  • Hoarseness

  • Excess mucus

  • Throat clearing

  • Globus

  • Cough

  • Dysphagia

  • Heartburn is RARE

Laryngopharyngeal Reflux- Diagnosis

  • Physical exam

    • Typically normal

  • Diagnostic tests

    • 24 hour pharyngo-esophageal pH monitoring

    • Nasopharyngolaryngoscopy

      • Erythema

      • Edema

      • Ulceration

Laryngopharyngeal Reflux- Treatment

  • Classic, non-pharmacologic GERD treatments

  • H2-blockers

  • Proton Pump Inhibitors


  • Control of airway inflammation in chronic asthma is critical for prevention/treatment of EIB

  • Maximize EIB control with attention to environment, behavior, and medications

  • Remember other causes of wheezing

  • Sports participation and exercise are both beneficial to all patients with asthma

  • Asthmatics compete and win at the highest levels in sports


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