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Exercise induced bronchoconstriction in adults: evidence based diagnosis and management

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• Peer review
• James M Smoliga , associate professor of physiology 1 ,
• Pnina Weiss , associate professor of pediatrics (respiratory) 2 ,
• Kenneth W Rundell , adjunct associate professor 3
• 1 Department of Physical Therapy, High Point University, High Point, NC 27268, USA
• 2 Pediatric Respiratory Medicine, Yale University School of Medicine, New Haven, CT 06520, USA
• 3 The Commonwealth Medical College, Scranton, PA, USA
• Correspondence to: J M Smoliga jsmoliga{at}highpoint.edu

What you need to know

Exercise induced bronchoconstriction (EIB) is most common in individuals with asthma but also occurs in those without

EIB is commonly misdiagnosed because its symptoms (such as shortness of breath, chest tightness, wheezing, and cough) are neither sensitive nor specific

EIB is most accurately diagnosed by using spirometry to measure forced expiratory volume in one second (FEV 1 ) before and after a high intensity exercise challenge in dry air or eucapnic voluntary hyperpnoea

Short acting β agonists are recommended first line treatment for confirmed EIB, used only “as required” rather than daily to avoid tolerance and potential exacerbations

People with EIB symptoms and a negative bronchoprovocation test or with documented EIB and ongoing symptoms despite treatment should have their management and diagnosis reviewed

Exercise induced laryngeal obstruction is a relatively common cause of breathlessness in athletes, which may mimic or occur alongside EIB

What is exercise induced bronchoconstriction (EIB)?

EIB is defined as “the transient narrowing of the lower airway following exercise in the presence or absence of clinically recognized asthma.” 1 Bronchoconstriction typically develops within 15 minutes after exercise and spontaneously resolves within 60 minutes. After an episode of EIB, there is often a refractory period of about 1-3 hours in which, if exercise is repeated, the bronchoconstriction is less emphasised in 40-50% of patients. 2 3 EIB can also occur during exercise. 4 5

The term “exercise induced bronchoconstriction” is preferred to that of “exercise induced asthma” since asthma is a chronic condition which is not induced by a single bout of exercise. EIB is more likely in people with asthma, but it also occurs in individuals without asthma. 1 6 EIB is characterised by falls in forced expiratory volume in one second (FEV 1 ) after exercise, while in people with asthma there is persistent airway inflammation and recurrent symptoms outside of exercise (that is, with allergen exposure or upper respiratory infections). Often, at baseline there is evidence of reversible lower airway obstruction. Pharmacological management for persistent asthma requires daily anti-inflammatory, preventive medications. However, airway inflammation and remodelling also occur in cold weather athletes with and without asthma and EIB. 7

We searched Medline for the terms “exercise induced bronchoconstriction” or “exercise induced asthma” or “asthma” and “athlete” or “exercise.” We also evaluated our personal archives of peer reviewed references. We gave priority to systematic reviews and meta-analyses, as well as professional society task force and practice parameter papers. When these comprehensive resources were insufficient or published more than five years ago, we used Google Scholar to identify more recent prospective epidemiological studies and randomised clinical trials which cited these references.

What triggers an episode of EIB?

EIB typically occurs after high intensity aerobic exercise during which high ventilation (>85% of maximal voluntary ventilation) dehydrates the respiratory mucosa and leads to a transient increase in airway osmolarity, mast cell activation with mediator release (including histamine, serine proteases, prostaglandins, and leukotrienes 8 ), and bronchoconstriction. Dry environments exacerbate EIB because of greater respiratory water loss. Exacerbations due to cold air are because of the reduced water content of the air rather than the low temperature. Increased exposure to allergens and respiratory irritants may exacerbate bronchoconstriction during high ventilation exercise. 9 EIB may be seasonal in some individuals with atopy, 10 11 although research on this association is limited. Figure 1 ⇓ shows the pathogenesis of EIB and how diagnostic tests and management interventions work.

Fig 1  Relation between pathophysiology of exercise induced bronchoconstriction (EIB), triggers of EIB attacks, diagnostic tests, and management strategies. (*Evidence from small studies suggests these interventions may reduce EIB severity, 12 13 14 but these may not be practical for athletes engaging in high intensity exercise)

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Who gets EIB?

EIB can occur in children and adults of various fitness levels, ranging from recreational to elite competitors, 15 16 with a reported prevalence of 10-50% or greater in high level athletes, depending on sport and surveillance or diagnostic methodology. 17 18 Individuals who are exposed to high concentrations of airborne particulate matter during high ventilation exercise have an increased incidence of EIB (see box 1).

Box 1: Athletes who show increased incidence of EIB when exposed to high concentrations of airborne particulate matter during high ventilation exercise 9

Individuals participating in physical activity in athletic fields and fitness trails adjacent to roads with high traffic volume

Those who regularly skate at ice rinks where ice resurfacers are powered by fossil fuels

Risks among winter sports athletes are increased by the dry ambient air

Swimmers who train in indoor chlorinated swimming pools experience inhalation exposure to chloramines (respiratory irritants that arise from the reaction of nitrogenous waste products with chlorine 19 )

How does EIB present?

Individuals with EIB typically complain of breathlessness, wheezing, cough, and chest tightness during or after exercise. Athletes may seek medical input because they feel that these symptoms limit their sports performance. However, the non-specific nature of the symptoms can make it hard to reach a firm diagnosis. A systematic review concluded that there are currently no questionnaires with sufficient sensitivity and specificity to diagnose EIB based on symptoms and signs alone. 20

How is EIB accurately diagnosed?

Algorithms for the diagnosis of EIB are available (see fig 2 ⇓ ). 1 8 18 21 Formal diagnosis requires either direct or indirect challenge tests designed to induce bronchoconstriction. Direct challenge uses a nebulised drug to stimulate the airway smooth muscle, whereas indirect challenge attempts to dehydrate the mucosa (see box 2). 22 Spirometry before and at 5, 10, 15, and 20 minutes after the stimulus measures the change in FEV 1 . A reduction of >10-15% in FEV 1 at two consecutive post-challenge time points is considered diagnostic for EIB, though specific recommendations vary (for example, the European Respiratory Society recommends a >12% fall in FEV 1 ). 18 Diagnostic thresholds are based on a greater post-challenge decrease in FEV 1 than that shown by 95-99% of the healthy population (2-3 standard deviations beyond the mean response). 23 About half of athletes with EIB will have a negative exercise challenge test result, so two tests may need to be done to exclude the diagnosis. 24

Fig 2  A simplified algorithm for evaluation and management of exercise induced bronchoconstriction (EIB). (*Ensure that a proper withholding schedule is followed (see table 1 ⇓ ). †Field tests may be attempted before laboratory tests: a positive field test is diagnostic for EIB, but false negative field tests are common, 27 28 so laboratory tests should be performed before EIB is excluded. ‡It may be necessary to perform an indirect test on two separate occasions before EIB can be ruled out. 24 §Ensure the patient is taking medication as directed.)

 Guidelines for withholding times of treatments before conducting challenge tests. Modified from Anderson et al 25 and Crapo et al 26

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Challenge tests are designed to trigger a bronchoconstriction and may provoke a severe attack. With the exception of the mannitol challenge, challenge tests should be conducted only in facilities where bronchodilator, supplementary oxygen, resuscitation equipment, and medical staff are readily available in the event of a severe response. 29 Direct and indirect challenge tests are contraindicated in patients with baseline impairments in FEV 1 (<70-80% of predicted).

Indirect tests are preferable to direct tests as they replicate the environmental conditions and the pathophysiology, including the inflammatory mediator release, that trigger respiratory symptoms. The most widely used indirect tests are high intensity exercise and eucapnic voluntary hyperpnoea (see box 2). Both tests use high ventilation rates in dry air conditions to dehydrate the respiratory mucosa. High intensity exercise has the advantage of exposing the individual to sport-specific physiological demands, whereas eucapnic voluntary hyperpnoea can be conducted in a controlled manner, which allows for easy standardisation between facilities.

Box 2: Challenge tests for EIB

Indirect challenge tests, high intensity exercise challenge.

Should be performed in a humidity controlled environmental chamber or by having the individual breathe medical grade compressed dry air (<5 mg H 2 O/L) throughout the exercise

Requires sufficient time spent at high intensity activity, with >90% maximal heart rate for the last 4 minutes of an 8 minute exercise challenge 1

>10% decrease in FEV 1 is a positive test

Eucapnic voluntary hyperpnoea

Performed with the patient hyperventilating for 6 minutes while breathing from a cylinder of medical grade compressed gas containing 4.9-5% CO 2 , 21% O 2 , balance N 2 29

Target ventilation of 30×FEV 1 or >85% of maximal voluntary ventilation (MVV), though >60% MVV is generally sufficient

For individuals who achieve a ventilation >60% MVV

- 10-19.9% decrease in FEV 1 is a mild response

- 20-29.9% decrease is a moderate response

- >30% decrease is severe 29

Mannitol challenge

Provides a safe alternative to the other tests because it allows clinicians to produce bronchoconstriction in a controlled and stepwise manner with increasing amounts of inhaled powdered mannitol, which increases osmolarity until a 15% decrease in FEV 1 occurs. 1 8 30 This reduces the risk of severe bronchoconstriction

Though useful in diagnosis, a negative mannitol challenge result is not sufficient to rule out EIB 8

Direct challenge tests

Direct stimulation involves the inhalation of nebulised methacholine in increasing concentrations until a given decrease (generally >15%) in FEV 1 is achieved

A negative test has a high negative predictive value (>90%) and can potentially rule out asthma and EIB. However, predictive value may be weaker in elite athletes and limits its clinical utility 31

What are the consequences of misdiagnosing EIB?

Diagnosis of EIB based on symptoms without proper adherence to established protocols has led to a high rate of false positive diagnoses, and consequent unnecessary use of bronchodilators. 32 However, individuals with false negative results (box 3) may not receive treatment and may continue to experience EIB. This may take the form of an occasional nuisance or severe impairment that causes them to stop taking part in sport and lose the health benefits of physical activity. 20 Though rare, there are reports of asthma related sudden death during sports participation, with one epidemiological study identifying 61 deaths in seven years in the United States. 35

Box 3: Common causes of false negative challenge results

Failure to expose the patient to sufficiently dry air 27

Insufficient exercise intensity (that is, <90% of maximum heart rate) 27

Performing a “confirmatory” challenge test while using previously prescribed medication based on symptoms. See table 1 ⇑ for details

Using a peak expiratory flow meter as a diagnostic tool instead of a spirometer (lacks appropriate sensitivity and positive predictive value 33 34 )

Test performed at the wrong time of the year in individuals with seasonal EIB 10 11

What can mimic EIB?

Other conditions can cause shortness of breath during exercise and may be mistaken for EIB. Asthma and exercise induced laryngeal obstruction (EILO, previously called vocal cord dysfunction) are two of the most common (see table 2 ⇓ ).

 Potential causes of breathlessness or exercise intolerance in athletes who do not have asthma or exercise induced bronchoconstriction (EIB)

Exercise induced laryngeal obstruction (EILO)

Some athletes experience EILO with or without EIB. 36 One study reported an incidence of 5% in 370 developmental or elite athletes, with about half of those with EILO also testing positive for EIB. 37 Among athletes referred for evaluation of asthma, about 35% had EILO, and, of these, approximately 39% also tested positive for EIB or asthma. 38 Thus, EILO and EIB are common comorbidities, but most individuals with EILO may not have EIB.

EILO often produces inspiratory stridor that can be confused with the wheeze of EIB. Stridor associated with EILO occurs during inspiration in the laryngeal region during exercise and resolves quickly after stopping exercise, whereas the wheeze associated with EIB typically occurs during exhalation after cessation of exercise. EILO should be considered in athletes who have symptoms of EIB but who test negative for it in bronchoprovocation testing, or in those who have documented EIB but continue to experience symptoms with exercise despite appropriate management. If EILO is suspected, the diagnosis can be confirmed with laryngoscopy during high intensity exercise, 39 and this may be performed simultaneously with a dry air challenge to test for concomitant EIB. 40

What are the treatment options for EIB?

Non-pharmacological management.

A systematic review and meta-analysis 2 found that, before vigorous intensity exercise, a warm-up procedure that included continuous high intensity activity (such as 6 minutes of hard uphill running) or sprint interval bouts reduced the later fall in FEV 1 . Although individuals vary in their airway response, athletes with EIB may wish to try including some sprint interval exercise (such as six to eight bouts of 30 second sprints with 45-120 seconds rest between 2 ) in their warm-up routine. Individuals with EIB may also try to avoid exercising in areas where they are exposed to high levels of air pollution and airborne allergens, and dry environments when possible.

Should people with EIB avoid exercise?

Exercise is of potential benefit to asthmatic patients with EIB and, if their asthma is well controlled, their exercise should not be limited. A systematic review and meta-analysis revealed that exercise training improved quality of life, reduced symptoms of asthma, decreased EIB and bronchial hyper-responsiveness, and attenuated the fall in FEV 1 . 41 Patients with EIB should be encouraged to continue taking exercise while adhering to their management plan, and should seek further medical evaluation if their symptoms do not resolve.

Pharmacological management

β agonists—People with EIB, with or without asthma, should be prescribed short acting (1-6 hours, depending on drug) β agonist bronchodilators, which should be used only as needed. Long acting β agonists are not used as sole therapy for either EIB or asthma because of the potential risk of severe asthma exacerbations and death. 42 A systematic review (including studies of adults and children with EIB) found that a single dose of a β agonist was effective in preventing EIB but confirmed that daily use leads to tolerance, which reduces its effectiveness as a rescue medication. 43 β agonists can be used before exercise two to four times a week to prevent bronchoconstriction or taken as a rescue inhaler as needed, but they should not be used daily. 1 8 44 If β agonists are needed more frequently, then a leukotrienes receptor antagonist (such as montelukast) or a daily inhaled corticosteroid should be considered. 1 8

Inhaled corticosteroids— Patients with known asthma who also have EIB should be managed with inhaled corticosteroids to reduce airway inflammation. Inhaled corticosteroids are most effective when administered daily and may take up to four weeks to reach maximal effectiveness. 1 8 44

Leukotrienes receptor antagonists— These cannot reverse bronchoconstriction but may prevent episodes of EIB if taken two hours before exercise. Protection can last for 24 hours, 1 8 but effectiveness varies widely between individuals. 45

Are any EIB treatments banned in elite athletes? Inhaled corticosteroids and some β agonists are now allowed, within certain limits, by the International Olympic Committee and World Anti-Doping Association (WADA), but some organisations, such as the National College Athletics Association (NCAA), still require a therapeutic use exemption (TUE). Leukotrienes receptor antagonists are allowed. Practitioners should be aware of organisation-specific requirements for documenting diagnosis and management.

What if symptoms persist despite treatment?

Health professionals should review the use of any short acting β agonist to ensure this is not being overused (risking tachyphylaxis) or underused. Inhaler technique should be reviewed. If there is no subjective improvement with treatment, patients should be offered repeat testing with spirometry or a repeat exercise challenge to provide objective measures of lung function and airway hyper-responsiveness. If symptoms persist despite these measures, the diagnosis should be re-evaluated.

When to refer

Facilities not available to perform dry air exercise challenge or EVH

Repeated negative result on properly conducted indirect challenge tests

Symptoms are not improved despite proper medication use

Non-reversible airway obstruction

Questions for future research

Can a screening questionnaire guide clinicians to differentiate EIB from other forms of breathlessness associated with exercise?

Can EIB phenotypes be categorised according to symptoms (such as individuals who cough but do not wheeze versus individuals who wheeze but do not cough), inflammatory cells or mediators, genetics (such as glutathione S-transferase polymorphisms), or environmental triggers (such as pollutant exposure versus dry and cold air exposure) in order to improve patient specific treatment strategies?

Why is it that, although EIB and EILO can exist independently, comorbidity is common?

Tiotropium bromide is used primarily for managing chronic obstructive pulmonary disease. It shows promise as an add-on therapy to decrease exacerbations and improve post-challenge FEV 1 in moderate to severe asthma. Could it be used for prophylaxis or rescue in patients with mild asthma or EIB without apparent asthma?

Tips for non-specialists

To avoid misdiagnosis, EIB should never be diagnosed on the basis of signs and symptoms alone

Diagnosis should include changes in FEV 1 before and after a challenge test

Positive field test results may be used to diagnoses EIB, but a negative field test result does not rule out EIB

Exercise challenge and eucapnic voluntary hyperpnoea tests should strictly adhere to guidelines and may need to be repeated

The nature and severity of clinical signs and symptoms of EIB should be fully documented before starting treatment. At diagnosis, clinicians should arrange a time to follow up the patient to determine whether interventions are successful

Additional educational information (freely available)

Parsons JP, Hallstrand TS, Mastronarde JG, et al. An official American Thoracic Society clinical practice guideline: exercise-induced bronchoconstriction. Am J Respir Crit Care Med 2013;187:1016-27— www.thoracic.org/statements/resources/allergy-asthma/exercise-induced-bronchoconstriction.pdf

Joint Task Force on Practice Parameters. Pathogenesis, prevalence, diagnosis, and management of exercise-induced bronchoconstriction: a practice parameter. Annal Allergy Asthma Immunol 2010;105:S1-47— www.aaaai.org/Aaaai/media/MediaLibrary/PDF%20Documents/Practice%20and%20Parameters/Exercise-induced-bronchoconstriction-2011.pdf

Carlsen KH, Anderson SD, Bjermer L, et al. Exercise-induced asthma, respiratory and allergic disorders in elite athletes: epidemiology, mechanisms and diagnosis: part I of the report from the Joint Task Force of the European Respiratory Society (ERS) and the European Academy of Allergy and Clinical Immunology (EAACI) in cooperation with GA2LEN. Allergy 2008;63:387-403— http://onlinelibrary.wiley.com/doi/10.1111/j.1398-9995.2008.01662.x/epdf

Carlsen KH, Anderson SD, Bjermer L, et al. Treatment of exercise-induced asthma, respiratory and allergic disorders in sports and the relationship to doping: Part II of the report from the Joint Task Force of European Respiratory Society (ERS) and European Academy of Allergy and Clinical Immunology (EAACI) in cooperation with GA(2)LEN. Allergy 2008;63:492-505— http://onlinelibrary.wiley.com/doi/10.1111/j.1398-9995.2008.01663.x/epdf

International Olympic Committee. IOC consensus statement on asthma in elite athletes: January 2008— www.olympic.org/Documents/Reports/EN/en_report_1301.pdf

Weiss P, Rundell KW. Imitators of exercise-induced bronchoconstriction. Allergy Asthma Clin Immunol 2009;5:7— www.aacijournal.com/content/pdf/1710-1492-5-7.pdf

Information resources for patients

American Academy of Allergy, Asthma & Immunology. Exercise and asthma. 2015— www.aaaai.org/conditions-and-treatments/library/asthma-library/exercise-and-asthma.aspx

Mayo Clinic. Diseases and conditions: Exercise-induced asthma— www.mayoclinic.org/diseases-conditions/exercise-induced-asthma/basics/definition/con-20033156

A patient’s story

I have had asthma and EIB most of my life. I also have an Olympic gold medal in women’s ice hockey. When I was younger, asthma did not hinder my lifestyle, and it was not a problem training with the US team in ice rinks resurfaced with electric powered machines. However, when we moved our training venue to a site that ice-resurfaced with fossil fuel powered equipment, my troubles began.

My doctors prescribed sodium cromoglicate, montelukast, and a rescue inhaler, and eventually inhaled corticosteroids. I did not like taking that medication, and was repeatedly non-compliant when I would start feeling better. I would then fall back into having asthma and EIB attacks. Just prior to the 2002 Olympics, I left the team and moved to New York City to coach ice hockey. I did not think I needed my medications any more. I was wrong and it was not long before I was having three severe asthma attacks daily and feeling like I was going to die.

I went to my doctor. The first resting spirometry manoeuvre triggered a response on the second, giving 25% predicted FEV 1 . I was in trouble! I am now compliant with medication, I have removed all triggers, and have been managing my asthma.

How patients were involved in the creation of this article

A patient story is included in this article

Cite this as: BMJ 2016;352:h6951

Contributors: JMS developed the idea for this article, performed the primary literature search, and wrote the majority of the article. PW and KWR wrote sections of the article, performed secondary literature searches, thoroughly reviewed drafts of the article, and approved its final contents. JMS is the guarantor of the article.

Competing interests: We have read and understood BMJ policy on declaration of interests and have no relevant interests to declare.

Provenance and peer review: Not commissioned; externally peer reviewed.

Patient consent: Patient consent obtained.

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• ↵ Rundell KW, Spiering BA, Baumann JM, Evans TM. Bronchoconstriction provoked by exercise in a high-particulate-matter environment is attenuated by montelukast. Inhal Toxicol 2005 ; 17 : 99 -105. OpenUrl CrossRef PubMed

Effects of physiotherapy treatment in patients with bronchial asthma: A systematic review

Affiliation.

• 1 Faculty of Physical Therapy, Universidade de Vigo, Spain.
• PMID: 32515632
• DOI: 10.1080/09593985.2020.1772420

Background : Bronchial asthma is a chronic inflammatory disease of the respiratory tract. Its physiotherapy treatment aims to reduce the frequency of asthmatic spells and the intensity of symptoms. The methods employed act mainly through the education of the patient in the correct handling of the asthma attacks and the improvement of the pulmonary elasticity. Objective : The objective of this review was to critically evaluate the available evidence on the effectiveness of different physiotherapy interventions in asthmatic patients. Methods : To achieve this, the search was focused on scientific databases with the key words Physiotherapy and Asthma. The search was limited to studies that evaluated the effects of a physiotherapy intervention in patients diagnosed with bronchial asthma. Results : 1794 articles were located and after the inclusion and exclusion criteria were applied, 12 studies were analyzed. Of these, 5 evaluated a respiratory reeducation intervention, 4 manual therapy techniques, 2 interventions based on therapeutic exercise and 1 relaxation techniques. Conclusions : The results obtained revealed that physiotherapy provides a wide range of treatment options for bronchial asthma and all of them provide positive results against the exclusive application of pharmacological treatment.

Keywords: Physical therapy modalities; asthma; pulmonary medicine.

Publication types

• Systematic Review
• Asthma* / therapy
• Exercise Therapy / methods
• Physical Therapy Modalities
• Respiratory Therapy

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• Published: 14 August 2018

Exercise-induced bronchoconstriction: prevalence, pathophysiology, patient impact, diagnosis and management

• Bhumika Aggarwal 1 ,
• Aruni Mulgirigama 2 &
• Norbert Berend 3 , 4  

npj Primary Care Respiratory Medicine volume  28 , Article number:  31 ( 2018 ) Cite this article

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• Respiratory signs and symptoms

Exercise-induced bronchoconstriction (EIB) can occur in individuals with and without asthma, and is prevalent among athletes of all levels. In patients with asthma, symptoms of EIB significantly increase the proportion reporting feelings of fearfulness, frustration, isolation, depression and embarrassment compared with those without symptoms. EIB can also prevent patients with asthma from participating in exercise and negatively impact their quality of life. Diagnosis of EIB is based on symptoms and spirometry or bronchial provocation tests; owing to low awareness of EIB and lack of simple, standardised diagnostic methods, under-diagnosis and mis-diagnosis of EIB are common. To improve the rates of diagnosis of EIB in primary care, validated and widely accepted symptom-based questionnaires are needed that can accurately replicate the current diagnostic standards (forced expiratory volume in 1 s reductions observed following exercise or bronchoprovocation challenge) in patients with and without asthma. In patients without asthma, EIB can be managed by various non-pharmacological methods and the use of pre-exercise short-acting β 2 -agonists (SABAs). In patients with asthma, EIB is often associated with poor asthma control but can also occur in individuals who have good control when not exercising. Inhaled corticosteroids are recommended when asthma control is suboptimal; however, pre-exercise SABAs are also widely used and are recommended as the first-line therapy. This review describes the burden, key features, diagnosis and current treatment approaches for EIB in patients with and without asthma and serves as a call to action for family physicians to be aware of EIB and consider it as a potential diagnosis.

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Introduction.

Exercise-induced bronchoconstriction (EIB) was first recognised as a condition in the 1960s, when it was noted that the forced expiratory volume in 1 s (FEV 1 ) in some patients with asthma fell below the resting level during and after exercise compared with other patients with asthma, whose FEV 1 returned to normal 10–15 min post exercise. 1 This phenomena was first given the term of exercise-induced asthma (EIA), 2 subsequently exercise-induced bronchospasm 3 and finally EIB in 1970. 4 The introduction of lung function tests, performed before and repeatedly after exercise, helped to identify EIB. 5 , 6 , 7 Cut-off points were introduced for FEV 1 (13% reduction) to reduce the likelihood of misclassifying children without EIB. 8 These methodologies led to the discovery that EIB was affected by environmental factors, such as air temperature and humidity. EIB symptoms were improved by inhaling humid air at ambient temperatures and were completely prevented by inhaling fully saturated air, warmed to body temperature. These experiments formed the basis of the heat vs osmotic hypothesis to describe EIB pathophysiology. 9 Today, updated international guidelines provide a summary of standard approaches to the diagnosis and management of EIB. 10 , 11 , 12

EIB mostly presents in patients with asthma, but can also be experienced by individuals without asthma, including athletes. 11 , 13 , 14 , 15 , 16 The number of patients with EIB is likely to be underestimated, due to the limited number of studies investigating the prevalence of EIB in patients both with and without asthma. This has contributed to a lack of awareness among physicians and the general population. 13 Access to effective diagnostic methods is limited, resulting in under- or mis-diagnosis. 13 In addition, there is a risk that physicians will misdiagnose EIB as asthma, and subsequently over- or undertreat the disease. Because EIB can restrict a patients’ ability to exercise and can negatively impact their quality of life (QoL), 14 , 17 there is a growing consensus that the management of EIB needs to be improved so that patients with the condition can continue to lead a physically active lifestyle. This review aims to increase awareness of EIB by providing an update on its burden, key features, diagnosis and current treatment approaches.

Definition and prevalence

EIB is defined as acute airway narrowing (which is transient and reversible) that occurs during or after exercise and can be observed in both patients who have and those who do not have chronic asthma. 11 , 18 Typical symptoms include dyspnoea, wheezing, cough, chest tightness, excessive mucus production or the feeling of a lack of fitness when the patient is in good physical condition. 12 , 13 EIB reportedly usually occurs within 2−5 min after exercise, peaks after 10 min and resolves in approximately 60 min.

Prevalence of EIB in the general population

The prevalence of EIB in the general population is approximately 5−20%. 19 , 20 , 21 , 22 , 23 However, because few epidemiological studies differentiate people with asthma from the general population, the true prevalence of EIB within the non-asthmatic general population is poorly understood. 12

The prevalence of EIB is greater in high-performance athletes than in the general population owing to prolonged inhalation of cold, dry air and airborne pollutants. 18 Studies have reported a prevalence of EIB among elite or Olympic-level athletes of 30–70%, 15 , 19 but reports are variable depending upon the environment in which the sport is performed, the type of sport and the maximum intensity achieved. 12

In children, the prevalence of EIB is also higher than in the general population, ranging from 3 to 35% (children ≤16 years old) (Fig. 1 ). 20 , 21 , 22 , 24 , 25 , 26 , 27 , 28 , 29 , 30 , 31 , 32 , 33 , 34 , 35 , 36 , 37 , 38 , 39 There is large variation in the prevalence of EIB in children worldwide, with studies conducted in Nigeria, 25 Brazil 30 and Poland 29 reporting higher rates of EIB than Ghana, 24 India 40 and Greece 26 (Fig. 1 ). The impact of ethnicity on the prevalence of EIB is unclear, as only one study has directly compared prevalence between different ethnic groups in Scottish and English children. 41 Children from an Asian background were 3.6 times more likely to experience EIB compared with Caucasian inner-city children. 41 The prevalence of EIB was 12.3% in children with Asian ethnicity compared with 9.1% in Afro-Caribbean children and 4.5% in Caucasian inner-city children. 41 These results should be interpreted with care because studies of ethnicity are invariably confounded by non-genetic factors.

Country-specific prevalence* of EIB in children (general population). 20 , 21 , 22 , 24 , 25 , 26 , 27 , 28 , 29 , 30 , 31 , 32 , 33 , 34 , 35 , 36 , 37 , 38 , 39 *Owing to differences in study methodology, comparisons between studies should be treated with caution. EIB exercise-induced bronchoconstriction

Children living in urban environments are 1.6 times more likely to experience EIB compared with those living in rural areas, based on a study conducted in Kenya. 22 The higher rates observed in urban areas were partially explained by an increased family history of asthma symptoms or increased exposure to environmental factors in urban areas, such as vehicle fumes, crowdedness and household animals. 22 Similar urban–rural difference were observed in India. In addition, children with a low or middle socio-economic status were 8–10% more likely to experience EIB than those with a high socio-economic status. 25 However, this finding is not universal; a study conducted in Nigeria demonstrated that EIB was not related to socio-economic class.

Prevalence of EIB in patients with asthma

Asthma is the main co-morbid factor associated with EIB, and EIB is estimated to occur in approximately 90% of patients with asthma. 12 , 19 Patients with poorly controlled or severe asthma are more likely to manifest with EIB than patients with well-controlled or milder disease. 12 , 19 Consequently, between-country differences in the prevalence of EIB should be considered in the context country-specific asthma control levels. 42 In children and adolescents with asthma, the prevalence of EIB is estimated to be approximately 20–90%, 29 , 30 , 35 , 38 with one study reporting that 46.7% of children with asthma display symptoms of EIB compared with 7.4% of those who do not have asthma. 30 The majority of patients with chronic asthma will likely experience a transient increase in symptoms following an appropriate exercise challenge. EIB is known to hinder children’s participation in vigorous activities. Other risk factors contributing to the prevalence of EIB include allergic rhinitis, a personal history of allergies, history of asthma in a close relative or history of wheeze. 20 , 21 , 30 , 35

Challenges of determining EIB prevalence and future work

It remains challenging to understand the extent of EIB within the general non-asthmatic population and among patients with asthma when such substantial variability in the prevalence of EIB is reported. This variability is likely due to differences in geographical regions and population characteristics (age, background, diagnosis of asthma) and differences in study design. The prevalence of EIB may be affected by the type of exercise test used to induce symptoms (treadmill, cycling, free running) or the diagnostic method used to define EIB (FEV 1 , peak expiratory flow (PEF), direct/indirect bronchial provocation tests or self-reported). 19 , 20 , 22 Moreover, the lung function index used (time of pre- and post-exercise measurements), temperature, seasons and humidity are also factors that may have affected prevalence data. 19 , 20 , 22 The influence of these factors highlights the need for standardised diagnostic measures to more accurately assess the prevalence of EIB. In addition, there is a pressing need for more epidemiological studies to assess the prevalence of EIB in the general population, excluding patients with asthma, to allow the prevalence of EIB without asthma to be better understood.

Pathophysiology

At present, the osmotic theory is widely accepted as the established underlying mechanism of EIB. The osmotic theory suggests that increased ventilation in the airways during periods of exercise leads to water loss from the airway surfaces by evaporation, thus dehydrating the airway surfaces and initiating the events that lead to the contraction of bronchial smooth muscle. 43 During exercise-related hyperventilation, transient osmotic change at the airway surface occurs owing to reductions in epithelium liquid volume, which in turn triggers mast cell degranulation. 43 Consequently, there is mast cell-mediated release of prostaglandins (prostaglandin D2), leukotrienes, histamine and tryptase. These signalling molecules are known to mediate airway smooth muscle contraction and increase mucus production and microvascular permeability and sensory nerve activation, and their release is thought to be the main stimulus for bronchoconstriction and airway oedema. 43

Precipitating factors for EIB

In patients with EIB and chronic asthma, the pathophysiological mechanisms described above simply represent a trigger of underlying airway hyperactivity associated with poorly controlled asthma. 44

On the other hand, in patients with EIB who do not have asthma, the mechanisms described by the osmotic theory are believed to be directly responsible for causing bronchoconstriction and associated symptoms. Intense ventilation of cold air can further increase dehydration of the airway surfaces and cause changes in bronchial blood flow, explaining why athletes performing in cold weather (e.g., ice hockey, Nordic skiing) demonstrate the highest rates of EIB. 10 , 45 Epithelial injury that is caused by the inhalation of air pollutants and poorly conditioned air during exercise has also been hypothesised to be a contributing factor for the development of EIB in patients without asthma. 46 , 47 This hypothesis likely explains why reported prevalence rates for EIB in competitive swimmers approach 50%, with exposure to chloramines from the pool water considered the probable cause of epithelial injury. 45 Supporting this theory, a family or personal history of atopy to environmental factors has been identified as a known risk for EIB. 45

Impact of EIB on patients

EIB is associated with both a physical and an emotional burden. From our review of the literature, we found that a limited number of studies have investigated the emotional burden associated with EIB. A large-scale, survey-based study of more than 30,000 children aged 6–14 years in Japan revealed that children self-reporting symptoms of EIB with or without asthma had significantly lower QoL scores than children without EIB ( p  < 0.001). 48 For children with asthma, the presence of EIB had a significant negative association with QoL regardless of the severity of asthma symptoms. 48 In the United States, adolescent athletes with or without asthma who reported dyspnoea during exercise ( n  = 32) showed significantly lower scores for health-related QoL (HRQoL), including sub-scores for physical functioning, general well-being and emotional functioning, than those without exercise-associated dyspnoea ( n  = 128). 49 However, adolescents with spirometry-defined EIB compared with non-spirometry-defined EIB in this study did not show significant reductions in HRQoL, possibly owing to the low number of patients included ( n  = 18). 49 A similar Swedish study of adolescents with or without asthma ( n  = 140) demonstrated a significant association between spirometry-defined EIB and reduced HRQoL. 50 Interestingly, this effect was revealed to be primarily driven by reduced total HRQoL and physical function in girls with EIB, with no significant difference evident between boys with or without EIB. 50 Girls with EIB also exhibited significantly higher scores for anxiety, but not depression, compared with girls without EIB. 50 A telephone-based survey, the Exercise-Induced Bronchospasm Landmark National Survey in the United States, provided comprehensive information relating to exercise-induced respiratory symptoms from the perspective of both the general population ( n  = 1085) and adults with EIB and asthma (defined as those who reported taking asthma medication in the previous year; n  = 1001). 14 The survey found a significant burden of disease associated with EIB, including emotional burden. 14 Patients with asthma who reported ≥1 symptom of EIB reported feeling more fearful (10.9 vs 27.7%; p  < 0.001), isolated (6.0 vs 15.1%; p  < 0.01), depressed (9.1 vs 23.4%; p  < 0.001), frustrated (22.9 vs 54.5%; p  < 0.001) and embarrassed (4.2 vs 20.0%; p  < 0.001) compared with those not reporting EIB symptoms. 14 While current evidence indicates a significant functional and emotional impairment among patients with EIB and asthma, there is a need for more studies to assess the burden of disease and HRQoL among patients with objectively measured EIB and underlying asthma, as well as among patients with EIB alone.

Almost half of patients (45.6%) with asthma reported impact on both their participation and performance in sports, and a similar number (42.7%) reported they could not keep pace with peers during physical activities. 14 A systematic review of studies assessing the impact of EIB on athletic performance failed to show a significant effect but did highlight the need for more well-designed, sport-specific studies on the physiological impact of EIB. 51

Impact of effective EIB management

Given the well-known health benefits of exercise in both the general population and individuals with asthma, 52 the need to manage EIB effectively is clear. Exercise, in particular swimming, 53 has been shown to improve lung function and asthma symptoms and outcomes, including QoL in patients with asthma. 54 An analysis of the impact of an aerobic training programme ( N  = 101) on asthma-specific health-related QoL, asthma symptoms, anxiety and depression scores in patients with moderate or severe persistent asthma found that aerobic training had an important role in the clinical management of persistent asthma. 54 Significant ( p  < 0.001) reductions in physical limitation and symptom frequency (Fig. 2 ) were reported in the training group compared with the control group. Moreover, only patients from the training group reported reductions in anxiety and depression levels ( p  < 0.001). 54

Impact of aerobic training on symptomatic burden in patients with moderate or severe persistent asthma. 54 Patients were 20–50 years old with moderate or severe persistent asthma. Patients were under medical treatment for 6 months and considered clinically stable; * p  < 0.05 compared with baseline; † p  < 0.05 compared with baseline and control group (two-way repeated-measure analysis of variance). Control group, n  = 45; aerobic training group n  = 44. **Time points are 0 days (1 month before treatment), 30 days (first month of treatment), 60 days (second month of treatment) and 90 days (third month of treatment) 54

Many patients stop exercising because of their EIB symptoms. In the 2011 EIB Landmark Survey, 22.2% of children with asthma aged 4−12 years and 31.8% of those aged 13−17 years avoided sports activities as a result of their EIB. As EIB affects up to 90% of patients with asthma, 12 the potential impact on aerobic exercise participation is substantial. Arguably, patients with asthma and EIB are at greater disadvantage than those with asthma and no EIB, for symptom precipitation during exercise often leads to avoidance of regular exercise and reduced QoL. It is important to raise awareness in primary care settings that EIB restricts exercise in patients with asthma, given the clinical and psychosocial benefits associated with physical activity.

The diagnosis of EIB in patients with and without asthma is multifactorial, leading to the condition often being either under- or over-diagnosed. 13 A recent systematic review found insufficient evidence to support the widespread adoption of any existing EIB screening tools, and highlighted that there exists a substantial unmet need for a validated questionnaire. 13 Here we will discuss a number of diagnostic methods that are currently used for diagnosing EIB in both patients with underlying asthma and in those with EIB alone.

EIB should be considered when patients report respiratory symptoms that are induced by exercise. One potential approach for family physicians is to ask the patient to measure his/her PEF after the typical exercise that usually provokes symptoms. 55 , 56 If peak flow results are reduced compared with the patient’s baseline readings, formal investigation is required. Diagnosis of EIB is confirmed based on specific changes in lung function provoked by exercise, rather than on the basis of symptoms. 11 , 18 Such testing can involve the use of both spirometric and bronchoprovocation techniques (Fig. 3 ; see refs. 11 , 18 , 44 , 47 , 57 ). 43

Algorithm for diagnosis of EIB. 11 , 18 , 44 , 47 , 57 EIB exercise-induced bronchoconstriction, FEV 1 forced expiratory volume in 1 s

The American Thoracic Society (ATS) Clinical Practice Guidelines outline a decline in FEV 1 of ≥10% from baseline after exercise or hyperpnoea challenge as confirmation of a positive EIB diagnosis. 11 A minimum of two reproducible FEV 1 measurements are taken in series post-exercise challenge, with the highest acceptable value being recorded at each interval (usually 5, 10, 15 and 30 min after exercise). The lowest percentage decline in FEV 1 within 30 min post exercise from the pre-exercise level can then be used to determine the severity of EIB (mild, 10– < 25%; moderate, 25– < 50%; severe ≥50%). 11

Bronchoprovocation testing

Many protocols recommend breathing dry air (10 mg H 2 O/L) with a nose clip in place while completing an exercise challenge. Several surrogates for exercise testing in the form of bronchoprovocation tests are available which, depending upon available resources, may be more suitable than a dry air exercise challenge. 11 The widely used methacholine challenge is a direct bronchoprovocation test; two versions of the methacholine challenge are used, a standard protocol recommended in ATS guidelines, and a second, more rapid protocol. 58 , 59 Alternatively, there are a number of indirect bronchoprovocation tests. The Eucapnic Voluntary Hyperventilation (EVH) test was developed specifically for identifying EIB. 60 Dry air (containing 5% carbon dioxide) is hyperventilated at room temperature for 6 min at a target ventilation of 30 times the subject’s FEV 1 , with a reduction of ≥10% of the pre-test value being diagnostic of EIB. 60 EVH testing is considered a reproducible, well-standardised test that is both quick and easy to administer; however, it is laboratory dependent and thus not widely available. 13 Other indirect bronchoprovocation tests include the hypertonic saline challenge and the mannitol test. 61 The latter was developed to improve the availability and standardisation of osmotic challenge testing; 62 , 63 however, the sensitivity and specificity of the mannitol challenge has yet to be well established. 11 , 13

While none of these bronchoprovocation tests are sensitive or specific to EIB, they all complement clinical history to identify airway hyperresponsiveness consistent with a diagnosis of EIB. 11 In addition, although these tests may be used for diagnosis of EIB in patients with and without underlying asthma, it has been suggested that indirect bronchoprovocation tests better reproduce the effects of exercise and may therefore be more accurate in diagnosing EIB in patients without asthma. 44

Distinguishing EIB from asthma

A key consideration for physicians when a patient presents with symptoms of wheeze and shortness of breath triggered by exercise is whether a diagnosis of asthma with EIB or EIB alone is appropriate. The management of EIB in patients without asthma is very different from the management of patients who experience EIB in association with poorly controlled asthma. As such, it is crucial to avoid over-diagnosis of asthma and subsequent over- or under-treatment.

The Global Initiative for Asthma (GINA) Guidelines outline several symptoms that increase or decrease the probability of a patient having asthma. 52 Most notably, symptoms that often worsen at night or in the early morning, that vary over time and in intensity, and that are triggered by exercise, viral infections, irritants and allergens increase the probability of asthma. Conversely, exercise-induced dyspnoea with noisy inspiration decreases the probability of asthma. 52 The guidelines also highlight the importance of determining if the patient’s symptoms occur only during or after exercise, and if the patient has any other risk factors for exacerbations. If symptoms are solely related to exercise, and there is no additional risk of exacerbation, a diagnosis of EIB rather than asthma should be considered. 52

Differential diagnosis

In the absence of airway hyperresponsiveness to challenge, differential diagnoses must be considered, particularly in adolescent athletes. Consideration must be given to the following conditions: bronchial hyperresponsiveness (the occurrence of cough or phlegm after intense exercise); exercise-induced vocal cord dysfunction (symptoms disappear when exercise is stopped and there is no observed effect of pre-exercise inhaled bronchodilator); and exercise-induced arterial hypoxaemia (occurring typically in well-trained athletes with high maximum oxygen uptake).

A Joint Task Force for defining practice parameters for the management of EIB (2016) suggested physicians can also consider cardiopulmonary exercise testing to determine if symptoms are resulting from exercise-induced dyspnoea and hyperventilation, particularly in children and adolescents. 43 Shortness of breath during exercise can also be associated with underlying conditions such as chronic obstructive pulmonary disease or restrictive lung conditions (e.g., obesity). 43 A history of shortness of breath alongside other systemic symptoms (e.g., pruritus, urticaria and hypotension) may rarely be indicative of exercise-induced anaphylaxis. 43 Finally, if EIB has been ruled out, referral to a specialist should be considered for patients who present as breathless when exercising (with or without chest pain) and for whom heart disease or other conditions are suspected. 43

Under-diagnosis and under-treatment

There is growing evidence that objectively confirmed EIB is more prevalent than would be assumed from using self-reported symptoms alone, 15 , 64 possibly because a decline in lung function post exercise (the criterion for EIB) may occur in the absence of symptoms. 23

A prospective study of varsity-level college athletes in the United States found that the use of symptoms to diagnose EIB is not predictive of whether athletes have objectively documented EIB. Of the 107 athletes included in the study, 42 (39%) recorded EVH results considered positive for EIB. 15 Of these athletes, 86% (36/42) reported no previous history of asthma. The EVH-confirmed prevalence of EIB was 36% in athletes without EIB symptoms compared with 35% in those with EIB symptoms. As such, the authors concluded that the empiric diagnosis and treatment of EIB following self-reported symptoms alone may result in an increase in inaccurate diagnoses and ultimately increased morbidity. 15 These results are corroborated by a study of elite British athletes, which showed that the majority (73%) with EVH-confirmed EIB were previously undiagnosed. 16

Failure to adequately diagnose EIB is also likely to result in under-treatment of symptoms. A survey conducted solely among patients with asthma found that although 83% of participants with asthma experienced at least one exercise-related respiratory symptom (shortness of breath, wheezing, coughing, difficulty taking a deep breath, noisy breathing or chest tightness during or immediately after exercising), only 30.6% reported a diagnosis of EIB. Importantly, despite these impairments, few respondents adhered to treatment guidelines relating to prophylactic medication prior to exercise. 14

Overall, current estimates reveal that approximately 70% of patients with asthma and EIB are diagnosed based on history and symptoms alone, and only 18% following exercise, medication or lung function testing (Table 1 65 ). A survey indicates that family physicians, in particular, are significantly less likely than pulmonologists to utilise objective testing for EIB. 66 This is likely to be due, at least in part, to access issues. Among family practitioners in England, 85% reported that they had no access to bronchoprovocation testing; 11% had access to laboratory-based exercise testing; and 4% had access to EVH, methacholine or mannitol provocation testing. 67

Treatment of EIB

Treatment of eib in patients without asthma.

For patients without underlying asthma, management of EIB should focus on relief of bronchoconstriction, and the reduction in risk (or prevention entirely) of the occurrence of bronchoconstriction, to allow the patient to continue to engage in physical exercise with minimal respiratory symptoms. There are many non-pharmacological approaches recommended to reduce the risk of bronchoconstriction, which include warm-up before exercise to induce a refractory period; interventions that pre-warm and humidify inhaled air during exercise (e.g., breathing through a face mask or scarf) and avoiding high exposure to air pollutants and allergens. 11 , 44 Some athletes use a physical warm-up of 10–15 min of moderately vigorous exercise before the planned period of exercise or competition to induce a so-called 'refractory period', during which EIB symptoms may be reduced. 43 If EIB symptoms continue despite these non-pharmacological approaches, use of pharmacological methods such as short-acting β 2 -agonists (SABAs) 15 min before exercise, leukotriene receptor antagonists (LTRAs) or chromones should be considered as alternative pre-exercise treatments in accordance with guidelines recommendations. 52

Treatment of EIB in patients with asthma

EIB in patients with asthma can be a sign of poor asthma control. In these cases, management of EIB should focus on following global treatment guidelines to ensure the underlying asthma is controlled. 52 Those patients who achieve good overall asthma control but retain EIB will require additional treatment. In addition to the non-pharmacological approaches described above, 11 guidelines recommend various pharmacological therapies to help prevent EIB in patients with chronic asthma.

Currently, patient understanding of EIB treatment may be characterised as inadequate. Only 22.2% of individuals experiencing exercise-related symptoms reported taking quick-relief medications prior to exercise ‘always’ or ‘most of the time’ (with this proportion increasing to just 38% in cases of diagnosed EIB).

The authors of the EIB Landmark Survey concluded that their findings highlighted an urgent need for better asthma education, with almost one-third of people with asthma reporting that they take rescue medication ≥3–6 times per week for uncontrolled asthma symptoms. 14 They suggest that exercise-related symptoms in this population reflect inadequate management of the underlying disease. Notably, 37% of patients with asthma were unaware that exercise-related symptoms indicate poor asthma control. 14 This finding highlights the need to confirm or refute a diagnosis of asthma as the first step in EIB management.

The ATS guidelines

The ATS guidelines 11 acknowledge that EIB may be present in both patients with and without asthma, and as such do not make specific recommendations based on the presence of asthma.

In patients diagnosed with EIB and asthma, the use of an inhaled SABA, typically 15 min before exercise, is strongly recommended 11 However, daily use of SABAs has been shown to lead to tolerance, and therefore should be used to prevent EIB on an intermittent basis only (i.e., less than daily on average). 11

Although not licensed specifically for EIB, the ATS recommends daily use of inhaled corticosteroids (ICS) for these patients, though it recognises that maximal improvement may require 2–4 weeks of treatment. The main benefit of ICS is as maintenance therapy to address underlying suboptimal control of asthma symptoms. The ATS recommendation against the use of a single dose of ICS immediately before exercise reflects this understanding. For patients who continue to have symptoms despite using an inhaled SABA before exercise, or who require an inhaled SABA daily or more frequently, daily use of long-acting β 2 -agonist (LABA) as a single therapy is not recommended due to known associations with acute exacerbations. 68 , 69 When EIB is unresponsive to SABA therapy, daily use of an LTRA taken at least 2 h before exercise or pre-exercise use of a mast cell stabiliser are recommended.

Guidelines on EIB by the Joint Task Force on Practice Parameters

This practice parameter summary is a 2016 update of contemporary practice guidelines first published in 2010 and based on a systematic literature review. 12 , 43 The updated guidelines recommend the use of SABAs for protection against EIB in both patients with and without asthma, and for accelerating recovery of pulmonary function. The Task Force recommends caution regarding the daily use of SABA alone or in combination with ICS for the management of EIB owing to the potential for tolerance (leading to a reduced duration/magnitude of effect). ICSs in combination with other preventive therapies are considered a good treatment option because of their ability to decrease the frequency and severity of EIB, although they do not necessarily eliminate it in patients with asthma. However, the guidelines do note that the use of ICS in the prevention of EIB in patients without asthma is controversial owing to a current lack of support from ad hoc designed clinical trials and impaired responses in patients with underlying neutrophilic inflammation. Consistent with the ATS guidelines, the use of daily LABAs with ICS therapy is not recommended for EIB unless this approach is needed to treat underlying moderate to severe persistent asthma.

Both LTRAs and mast cell-stabilising agents are considered suitable pre-exercise treatment options. 43 Inhaled ipratropium bromide should be considered for patients who have not responded to other agents; however, its ability to attenuate EIB is considered inconsistent. 43

Recommended treatment options: the evidence

Short-acting β 2 -agonists.

SABAs are the single most effective therapeutic agents for the acute prevention of intermittent EIB 43 (Fig. 4 ). SABAs stimulate β 2 -receptors on the surface of the airway smooth muscle, causing relaxation and bronchodilation, as well as possibly preventing mast cell degranulation. 11 In patients' asthma and EIB, SABAs have been shown to be effective in preventing a fall in FEV 1 (Fig. 4 ). 70 Evidence shows that when combined with pre-exercise warm-ups, SABAs still provide an additive protective effect in patients with asthma and EIB 11 and confer a greater protective effect against developing EIB than either warm-up or SABA alone. 71

Mean values for forced expiratory volume in 1 s in patients with exercise-induced asthma treated with a short-acting β 2 -agonist. 70 Data are expressed as a percentage of the predicted normal value, measured before and 30 min after each treatment and for 15 min after exercise. Crossover study conducted in 27 patients. Reproduced from Anderson et al. (2001) with permission from Wolters Kluwer Health, Inc. DPI dry powder inhaler, FEV 1 forced expiratory volume in 1 s, pDMI pressurised metered dose

Inhaled corticosteroids

A Cochrane review of results from eight randomised controlled trials involving 162 participants found that ICS taken for 4 weeks pre-exercise can reduce post-exercise declines in FEV 1 in both children and adults. 72 ICS is licensed only for patients with asthma and may not be as effective against EIB alone. One study noted that EIB symptoms were unchanged in the majority (67%) of patients with EIB alone following a mean of 22 weeks of ICS therapy. 48

Long-acting β 2 -agonists

The LABA formoterol has also been shown to provide improvements in EIB and but daily use of LABAs with ICS therapy is not recommended for EIB unless to treat underlying moderate to severe persistent asthma. 12 , 43 , 11 Comparisons of SABAs and LABAs (salmeterol) in patients ( N  = 12) with mild-to-moderate stable asthma showed that both treatments reduced mean declines in FEV 1 following exercise, with the SABA (3.8 ± 5.5%) and LABA (0.83 ± 6.2%) showing large effects 1 h post challenge compared with placebo (27.1 ± 7.3%). 73 However, a meta-analysis has demonstrated that the bronchoprotective effect of salmeterol at 9 h post treatment is reduced after 4 weeks. 74

Leukotriene receptor antagonists

Finally, LTRAs have also been shown to be efficacious for EIB in patients with and without asthma; LTRAs are also specifically indicated for prophylaxis in patients with asthma and EIB. 75 Clinical data have shown that once-daily treatment with montelukast (5 or 10 mg tablet) can improve a number of post-exercise deficits in lung function within 3 days in some patients. 76 In a pooled analysis of seven trials, patients with asthma and EIB had a mean maximum decline in post-exercise FEV1 that was 10.7% less with LTRAs compared with placebo. 11

Treatment of EIB in athletes

The treatment of EIB in elite athletes is a topic of particular interest and one that falls outside the scope of this review. Diagnosis and treatment of EIB in elite athletes has been extensively covered by a Joint Task Force Report prepared by the European Respiratory Society, the European Academy of Allergy and Clinical Immunology and GALEN, 10 as well as the World-Anti-Doping Agency. 77 Notably, the International Olympic Committee recommend that treatment follows international guidelines as described above; ICS and some inhaled SABAs can be used in accordance with the Therapeutic Use Exemption Standard. 78 In addition, athletes should be warned of the diminishing therapeutic effects of inhaled SABAs when used frequently, and offered education in order to develop self-management skills and ensure appropriate use of medication.

Conclusions

EIB can occur in both patients with and without asthma, with the prevalence in patients with asthma estimated at approximately 90%. 12 EIB may lead to a substantial emotional burden on patients, and restrict exercise and sports participation. This potentially leads to long-term QoL and physical health consequences in patients with EIB, with or without asthma. Increased awareness among patients and physicians of the symptoms and risk factors for EIB and increased use of objective diagnostic tests is key to the holistic management of patients with EIB. As such, there is a pressing need for more research into EIB in patients with and without asthma, and the development of validated and widely acceptable screening methods and/or accurate diagnostic methods, which can be made accessible to family physicians.

For patients with and without asthma, pre-exercise SABAs are recommended as the first-line option for pharmacological treatment of EIB. 11 , 43 The primary focus should be to increase awareness of EIB and educate patients to recognise symptoms and risk factors of EIB. Improved diagnosis and patient education further helps to optimise symptom control. Furthermore, increasing the accuracy of EIB diagnoses and providing education in how the patient can use SABA to prevent symptoms are needed.

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Aggarwal, B., Mulgirigama, A. & Berend, N. Exercise-induced bronchoconstriction: prevalence, pathophysiology, patient impact, diagnosis and management. npj Prim Care Resp Med 28 , 31 (2018). https://doi.org/10.1038/s41533-018-0098-2

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EXERCISE-INDUCED ASTHMA OVERVIEW

Exercise-induced asthma occurs when the airways narrow as a result of exercise. The preferred term for this condition is exercise-induced bronchoconstriction (EIB); exercise does not cause asthma, but is frequently an asthma trigger.

A person may have asthma symptoms that become worse with exercise (more common) or may have only exercise-induced bronchoconstriction, without symptoms at other times. If a person's asthma is triggered only during vigorous exercise (exercise-induced bronchoconstriction), they are considered to have mild intermittent asthma. Separate topic reviews discuss asthma in children and adults. (See "Patient education: Asthma treatment in adolescents and adults (Beyond the Basics)" and "Patient education: Asthma symptoms and diagnosis in children (Beyond the Basics)" .)

EXERCISE-INDUCED ASTHMA SYMPTOMS

Typical symptoms are shortness of breath, chest tightness, and cough. Exercise-triggered symptoms typically develop 10 to 15 minutes after a brief episode of exercise or about 15 minutes into prolonged exercise. Symptoms typically resolve with rest over 30 to 60 minutes. Exercise-induced symptoms occur more commonly and are more intense when the inhaled air is cold, probably due to changes in the airways that are triggered by the large amounts of relatively cool, dry air inhaled during vigorous activity. (See "Patient education: Trigger avoidance in asthma (Beyond the Basics)" .)

EIB is different than simple shortness of breath related to exercise, which generally resolves within five minutes of stopping exercise.

EXERCISE-INDUCED ASTHMA PREVENTION

Exercise is important for your health, even if you have asthma, so it is important to develop a routine that allows exercise. Some patients can often prevent or reduce exercise-induced asthma symptoms by improving their day-to-day asthma control and improving their fitness level with regular exercise.

Nonmedical preventive methods  —  Breathing cold, dry air during exercise can provoke asthma symptoms. Wearing a loosely fitting scarf or mask when exercising in cold, dry air or exercising where the air is warmer and more humid can help prevent exercise-induced asthma symptoms. Some patients find that warm-up routines before intense exertion can help reduce asthma symptoms.

For people who exercise once a day or less  —  Preventing exercise-induced bronchoconstriction usually includes use of an inhaled medication prior to exercise.

Rapid-acting bronchodilators  —  Inhalation of a rapid-acting bronchodilator (eg, two puffs of albuterol) may be taken 5 to 20 minutes before exercise. This inhaler can also be used to relieve symptoms caused by exercise. (See "Patient education: Asthma inhaler techniques in children (Beyond the Basics)" and "Patient education: Inhaler techniques in adults (Beyond the Basics)" .)

An alternative is to use a combination inhaler that includes formoterol and an inhaled corticosteroid. Formoterol works as quickly as albuterol and lasts for 12 hours, so it is both a rapid-acting and a long-acting bronchodilator. For prevention of exercise-induced asthma one of the combination inhalers, such as budesonide-formoterol (brand names: Breyna, Symbicort) or mometasone-formoterol (brand name: Dulera), can be used one inhalation, at least five minutes prior to exertion. Like albuterol, these medications can also be used to relieve asthma symptoms.

For exertion throughout the day  —  Some adults and most children exercise intermittently throughout the day, making it hard to use a preventive treatment before each episode of activity. In this case, a long-acting inhaled bronchodilator (eg, salmeterol or formoterol) or a leukotriene modifier (eg, montelukast or zafirlukast) may be recommended to provide day-long protection (see 'Leukotriene modifiers' below).

Long-acting bronchodilators  —  Long-acting bronchodilators (LABAs), such as salmeterol and formoterol, work for a longer period than rapid-acting bronchodilators. LABAs should always be used in combination with an inhaled glucocorticoid. While formoterol is a LABA, it works as quickly as albuterol. Combination inhalers containing formoterol can be used shortly before exercise (at least five minutes) and can also be used to relieve asthma symptoms that occur despite pretreatment.

Some patients prefer to take their inhaler on a once or twice a day schedule. In this case, inhalers that contain the LABA, salmeterol, and an inhaled corticosteroid (eg, Advair or Seretide in Europe) can be used. These medications are usually taken twice daily and 30 minutes after the morning dose help prevent exercise-induced asthma symptoms for the next 12 hours.

Leukotriene modifiers  —  Leukotriene modifiers work by decreasing airway narrowing, inflammation, and mucus production. Examples of leukotriene modifiers include montelukast (brand name: Singulair) and zafirlukast (brand name: Accolate). These are taken in pill form by mouth once daily (montelukast) or twice daily (zafirlukast) and have few side effects. Taken regularly, either of these medications is useful in preventing exercise-induced bronchospasm.

Leukotriene modifiers may be used as an alternative to rapid-acting bronchodilators to prevent exercise-induced bronchoconstriction for patients who prefer or need all-day protection or have difficulty using inhalers.

Montelukast is approved for use as needed before exercise for patients who do not require daily medication. If not taken on a daily basis, montelukast should be taken at least two hours before the start of exercise. If the medication is taken daily, there is no need to take an additional dose prior to exercise.

Leukotriene modifiers are used for prevention of symptoms, NOT for relief of symptoms once they have developed. If asthma symptoms develop despite pretreatment with a leukotriene modifier, a rapid-acting bronchodilator (eg, albuterol, levalbuterol, or budesonide-formoterol) should be used.

ASTHMA ATTACK TREATMENT

The term "asthma attack" is somewhat confusing because it does not distinguish between a mild increase in symptoms and a life-threatening episode. Asthma symptoms may develop during exercise despite pretreatment and may sometimes be more severe than expected. Exercise induced asthma symptoms may be aggravated by changes in air quality, common colds, exposure to allergens, or changes in the weather. These triggers can cause mild, moderate, or severe symptoms to develop. Any of these changes could be considered an asthma "attack."

Some people have periodic, mild attacks that never require emergency care, while others have severe and sudden attacks that require a call for emergency medical services.

Emergency care plan  —  A patient or parent/caregiver should work with a healthcare provider to formulate an emergency care plan (also called an asthma action plan) that explains specifically what to do if asthma symptoms worsen.

● Mild attacks – Take your rescue medication: most people take two puffs of albuterol or levalbuterol, or one puff of formoterol-budesonide. This may be repeated twenty minutes later, and then periodically (every two to four hours) until symptoms are improved. People who take controller medications, such as inhaled glucocorticoids, may need to increase the dose and should contact their provider for further instruction.

● Severe attack – Take two to six puffs of a rescue medication, depending upon how much the individual can tolerate at once without becoming too jittery. For patients with home nebulizer machines, two treatments can be given, 20 minutes apart.

For severe symptoms or symptoms that worsen or do not improve after initial use of a rescue medication, someone should immediately call for emergency medical assistance. Severe asthma attacks can be fatal if not treated promptly.

In most areas of the United States, emergency medical assistance is available by calling 911. Patients should not attempt to drive to the hospital and should not ask someone else to drive. Calling 911 is safer than driving for two reasons:

● From the moment EMS personnel arrive, they can begin evaluating and treating asthma. When driving in a car, treatment cannot begin until the person arrives in the emergency department.

● If a dangerous complication of asthma occurs on the way to the hospital, EMS personnel may be able to treat the problem immediately.

Following a severe asthma attack, the patient is usually given a three to ten day course of an oral glucocorticoid medication (eg, prednisone, prednisolone). This treatment helps to reduce the risk of a second asthma attack.

Wear medical identification  —  Many people with medical conditions wear a bracelet, necklace, or similar alert tag at all times. If an accident occurs and the person cannot explain their condition, this will help responders provide appropriate care.

The alert tag should include a list of major medical conditions and allergies, as well as the name and phone number of an emergency contact. One device, Medic Alert ( www.medicalert.org ), provides a toll-free number that emergency medical workers can call to find out a person's medical history, list of medications, family emergency contact numbers, and healthcare provider names and numbers.

WHERE TO GET MORE INFORMATION

Your healthcare provider is the best source of information for questions and concerns related to your medical problem.

This article will be updated as needed on our web site ( www.uptodate.com/patients ). Related topics for patients, as well as selected articles written for healthcare professionals, are also available. Some of the most relevant are listed below.

Patient level information  —  UpToDate offers two types of patient education materials.

The Basics  —  The Basics patient education pieces answer the four or five key questions a patient might have about a given condition. These articles are best for patients who want a general overview and who prefer short, easy-to-read materials.

Patient education: Exercise-induced asthma (The Basics) Patient education: Asthma in adults (The Basics) Patient education: Asthma in children (The Basics)

Beyond the Basics  —  Beyond the Basics patient education pieces are longer, more sophisticated, and more detailed. These articles are best for patients who want in-depth information and are comfortable with some medical jargon.

Patient education: Asthma treatment in adolescents and adults (Beyond the Basics) Patient education: Asthma symptoms and diagnosis in children (Beyond the Basics) Patient education: Trigger avoidance in asthma (Beyond the Basics) Patient education: Asthma inhaler techniques in children (Beyond the Basics) Patient education: Inhaler techniques in adults (Beyond the Basics)

Professional level information  —  Professional level articles are designed to keep doctors and other health professionals up-to-date on the latest medical findings. These articles are thorough, long, and complex, and they contain multiple references to the research on which they are based. Professional level articles are best for people who are comfortable with a lot of medical terminology and who want to read the same materials their doctors are reading.

Antileukotriene agents in the management of asthma An overview of asthma management in children and adults Beta agonists in asthma: Acute administration and prophylactic use Exercise-induced bronchoconstriction Trigger control to enhance asthma management Asthma education and self-management

The following organizations also provide reliable health information.

● The National Library of Medicine

     ( www.nlm.nih.gov/medlineplus/healthtopics.html )

● National Heart, Lung, and Blood Institute

     ( www.nhlbi.nih.gov/ )

● American Lung Association

     ( https://www.lung.org/ )

● The Asthma and Allergy Foundation of America

     ( www.aafa.org )

● American Academy of Allergy, Asthma, and Immunology

     ( www.aaaai.org/patients.stm )

● American College of Allergy, Asthma, and Immunology

     ( https://acaai.org/asthma/types-of-asthma/exercise-induced-bronchoconstriction-eib/ )

• Global Initiative for Asthma. The Global Strategy for Asthma Management and Prevention. https://ginasthma.org/ (Accessed on June 29, 2021).
• Weiler JM, Brannan JD, Randolph CC, et al. Exercise-induced bronchoconstriction update-2016. J Allergy Clin Immunol 2016; 138:1292.
• Philip G, Villarán C, Pearlman DS, et al. Protection against exercise-induced bronchoconstriction two hours after a single oral dose of montelukast. J Asthma 2007; 44:213.
• Parsons JP, Hallstrand TS, Mastronarde JG, et al. An official American Thoracic Society clinical practice guideline: exercise-induced bronchoconstriction. Am J Respir Crit Care Med 2013; 187:1016.
• Boulet LP, O'Byrne PM. Asthma and exercise-induced bronchoconstriction in athletes. N Engl J Med 2015; 372:641.
• Lazarinis N, Jørgensen L, Ekström T, et al. Combination of budesonide/formoterol on demand improves asthma control by reducing exercise-induced bronchoconstriction. Thorax 2014; 69:130.

Exercise-induced asthma

On this page, alternative medicine, preparing for your appointment.

To diagnose exercise-induced bronchoconstriction, your health care provider first takes a medical history and does a physical exam. You may have tests to check your lung function and rule out other conditions.

Test of current lung function

Your provider will likely perform a spirometry (spy-ROM-uh-tree) test. This exam shows how well your lungs function when you aren't exercising. A spirometer measures how much air you inhale, how much you exhale and how quickly you exhale.

Your provider might have you repeat the test after you take an inhaled medicine to open your lungs. This medicine is known as a bronchodilator. Your provider compares the results of the two measurements to see whether the bronchodilator improved your airflow. This initial lung function test is important for ruling out chronic asthma as the cause of symptoms.

A spirometer is a diagnostic device that measures the amount of air you're able to breathe in and out. It also tracks the time it takes you to exhale completely after you take a deep breath.

Exercise challenge tests

During an exercise challenge test, you run on a treadmill or use other stationary exercise equipment to increase your breathing rate.

The exercise needs to be intense enough to trigger your symptoms. If needed, you might be asked to perform a real-life exercise challenge, such as climbing stairs. Spirometry tests before and after the challenge can provide evidence of exercise-induced bronchoconstriction.

Methacholine challenge breathing test

This test involves inhaling an agent, often methacholine, that narrows the airways in some people with exercise-induced bronchoconstriction. Afterward, a spirometry test checks lung function. This test mimics the conditions likely to trigger exercise-induced bronchoconstriction.

Your health care provider might prescribe medicines to take shortly before exercise or to take daily for long-term control.

Preexercise medicines

If your provider prescribes a medicine to take before exercising, ask how much time you need between taking the medicine and starting the activity.

• Short-acting beta agonists (SABAs) are the most commonly prescribed medicines to take before exercising. These medicines include albuterol (ProAir HFA, Proventil-HFA, Ventolin HFA) and levalbuterol (Xopenex HFA). short-acting beta2 agonists (SABAs) are inhaled medicines that help open airways. Do not use these medicines every day because it can make them less effective.
• Ipratropium (Atrovent HFA) is an inhaled medicine that relaxes the airways and may be effective for some people. A generic version of ipratropium also can be taken with a device called a nebulizer.

Long-term control medicines

Your provider may prescribe a long-term control medicine to manage underlying asthma or to control symptoms when preexercise treatment alone doesn't work. These medicines are usually taken daily. They include:

• Inhaled corticosteroids, which help calm inflammation in your airways. You take these medicines by breathing them in. You might need to use this treatment for up to four weeks before it will have maximum benefit.
• Combination inhalers, which contain a corticosteroid and a long-acting beta agonist (LABA), a medicine that relaxes airways. These inhalers are prescribed for long-term control, but your provider may recommend using it before you exercise.

Leukotriene modifiers, which are medicines that block inflammatory activity for some people. These medicines are taken by mouth. They can be used daily or before exercise if taken at least two hours in advance.

Possible side effects of leukotriene modifiers include behavior and mood changes and suicidal thoughts. Talk to your provider if you have these symptoms.

Don't rely only on quick-relief medicines

You also can use preexercise medicines as a quick-relief treatment for symptoms. However, you shouldn't need to use your preexercise inhaler more often than recommended.

Keep a record of:

• How many puffs you use each week.
• How often you use your preexercise inhaler for prevention.
• How often you use it to treat symptoms.

If you use your inhaler daily or you frequently use it for symptom relief, your provider might adjust your long-term control medication.

Exercise is an important part of a healthy lifestyle for everyone, including most people with exercise-induced bronchoconstriction. Besides taking your medicine, you can take these steps to prevent or reduce symptoms:

• Do about 15 minutes of warmup that varies in intensity before you begin regular exercise.
• Breathe through your nose to warm and humidify air before it enters your lungs.
• Wear a face mask or scarf when exercising, especially in cold, dry weather.
• If you have allergies, avoid triggers. For example, don't exercise outside when pollen counts are high.
• Try to avoid areas with high levels of air pollution, such as roads with heavy traffic.

If your child has exercise-induced bronchoconstriction, talk to your health care provider about providing an action plan. This document provides step-by-step instructions for teachers, nurses and coaches that explain:

• What treatments your child needs.
• When treatments should be given.
• What to do if your child has symptoms.

There is limited clinical evidence that any alternative treatments benefit people with exercise-induced bronchoconstriction. For example, it's been suggested that fish oil, vitamin C or vitamin C supplements can help prevent exercise-induced bronchoconstriction, but there isn't enough evidence to show if they're useful.

You're likely to start by seeing your primary health care provider. Your provider may refer you to someone who specializes in asthma, such as an allergist-immunologist or a pulmonologist.

Be prepared to answer the following questions:

• What symptoms have you had?
• Do they start immediately when you start exercising, sometime during a workout or after?
• How long do the symptoms last?
• Do you have breathing difficulties when you're not exercising?
• What are your typical workouts or recreational activities?
• Have you recently made changes to your exercise routine?
• Do the symptoms occur every time you exercise or only in certain environments?
• Have you been diagnosed with allergies or asthma?
• What other medical conditions do you have?
• What medications do you take? What is the dosage of each medication?
• What dietary supplements or herbal medications do you take?

Dec 07, 2022

• Exercise-induced bronchoconstriction (EIB). American College of Allergy, Asthma & Immunology. https://acaai.org/asthma/types-of-asthma/exercise-induced-bronchoconstriction-eib/. Accessed Oct. 21, 2022.
• Klain A, et al. Exercise-induced bronchoconstriction in children. Frontiers in Medicine. 2022; doi:10.3389/fmed..
• Malewska-Kaczmarek K, et al. Adolescent athletes at risk of exercise-induced bronchoconstriction: A result of training or pre-existing asthma? International Journal of Environmental Research and Public Health. 2022; doi:10.3390/ijerph19159119.
• Pigakis KM, et al. Exercise-induced bronchospasm in elite athletes. Cureus. 2022; doi:10.7759/cureus.20898.
• Asthma and physical activity in the school. National Heart, Lung, and Blood Institute. https://www.nhlbi.nih.gov/resources/asthma-and-physical-activity-school. Accessed Oct. 27, 2022.
• Broaddus VC, et al., eds. Exercise testing. In: Murray and Nadel's Textbook of Respiratory Medicine. 7th ed. Elsevier; 2022. https://www.clinicalkey.com. Accessed Oct. 27, 2022.
• Burks AW, et al. Asthma pathogenesis. In: Middleton's Allergy: Principles and Practice. 9th ed. Elsevier; 2020. https://www.clinicalkey.com. Accessed Oct. 27, 2022.
• O'Byrne PM. Exercise induced bronchoconstriction. https://www.uptodate.com/contents/search. Accessed Oct. 27, 2022.
• FDA requires Boxed Warning about serious mental health side effects for asthma and allergy drug montelukast (Singulair); advises restricting use for allergic rhinitis. Food & Drug Administration. https://www.fda.gov/drugs/drug-safety-and-availability/fda-requires-boxed-warning-about-serious-mental-health-side-effects-asthma-and-allergy-drug. Accessed Oct. 27, 2022.
• Li JT (expert opinion). Mayo Clinic. Oct. 31, 2022.
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