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Design
A mixed methods design, which combined qualitative and quantitative data was used in the present study. The data were gathered before and after a five months intervention period in the eighteen participants. The qualitative material is descriptive and consists of a) recordings of subjective experiences of respiratory distress explored via a questionnaire also used by Roksund [30], and b) qualitative descriptions of the findings of the body examinations. Quantitative measurements include objective measures of lung function and aerobic capacity. Each participant had between eight and twelve physiotherapeutic consultations during the intervention.
Participants
Inclusion criteria were adolescent athletes with symptoms of EILO and who were referred to NPMP treatment. Twenty two adolescent athletes between 13 – 19 years who were referred to NPMP treatment due to shortness of breath and possibly EILO between December 2018 and August 2022 were asked by the physiotherapist to take part in the study. Eighteen of these athletes (17 females, 1 male) were included. Before inclusion, they were subjected to an introductory interview based on the questionnaire developed by Roksund [30] to determine whether their symptoms were indicative of EILO. Exclusion criteria were additional diagnosis or respiratory symptoms not adhering with EILO. Four athletes referred to NPMP due to possible EILO were not included due to additional diagnosis.
The participants were referred by doctors or paediatrics working with respiratory problems in children and adolescents. Laryngeal movements had been measured using a continuous laryngoscopy exercise test (CLE) [31, 32] to verify the condition in four participants. Subjective experiences of inspiratory distress located in the larynx area during physical activity and recordings in the questionnaire confirmed the EILO condition in all participants.
Recordings of respiratory distress
Subjective experiences of respiratory distress were explored pre and post intervention through a comphrehensive history taking and in the interview based on the questionnaire previously used by Roksund to obtain the medical history, level of engagement in sport, information of symptoms related to exercise, activity level of the subjects and the influence of the symptoms on daily life [30]. A visual analogue scale served to grade the severity of symptoms (see Table 2).
The Body examination
The intervention was based on a thorough body examination commonly used in NPMP in which bodily imbalances in general and restrictions associated with the breathing in particular were assessed. The observations conducted by the physiotherapist during the body examinations were assessed and noted qualitatively and descriptively. They were not graded, since we did not use examination methods that grades the findings, but assessed and descriptively described the respiration, posture, muscular tension and functioning, the latter indicating bodily flexibility and ability to relax.
Measure of lung function and cardiac respiratory fitness
Lung function was measured by maximal expiratory flow-volume curves and ventilatory capacity by maximal voluntary ventilation (MVV) (MasterScreen Pneumo spirometer; CareFusion, Hochberg, Germany) according to current guidelines [33]. Lung function is presented as forced vital capacity (FVC) and forced expiratory volume in 1 s (FEV1). Lung function was measured before and 1, 3, 6 and 10 min after exercise test and a reduction of ≥ 10% in FEV1 was defined as exercise induced bronchial constriction (EIB).
Exercise test. Maximal oxygen consumption (VO2max) was measured using a mixing-chamber gas analysis system (OxyconPro analyzer; Jaeger, Würtzburg, Germany) on a treadmill (ELG 90/200 Sports; Woodway, Weil am Rhein, Germany). Prior to the test, the participants performed a 10 min standardized warm-up, tailored to the individual. Output speed was adjusted to the participant’s fitness level, and the speed was thereafter increased by 1 km·h−2 every minute until voluntary exhaustion. The incline was set to 5% and did not change during the test. VO2max was defined as the mean of the two highest 30 s measurements coupled with a maximal respiratory exchange ratio (RERmax) > 1.1. The following variables were extracted and included in the analyses; VO2max, maximal minute ventilation (VEmax), maximal breathing frequency (BFmax), RERmax, maximal heart rate (HRmax), time to exhaustion and Borg scale for self-perceived exhaustion. Breathing reserve (BR) (%) was estimated as MVV-VEmax/100 × 100.
The intervention
The intervention had a multidimensional approach that included physiotherapy, elements of cognitive behavioural therapy and an individually tailored rehabilitation plan, all handled by the first author (who has a PhD in sports science and is a certified NPMP specialist) in close collaboration with the participants and their parents.
A: The physiotherapy intervention
Was based on the main principles of NPMP and addressed bodily and respiratory restrictions identified in the body examinations. Intervention details were recorded during each consultation. The NPMP approach differs from traditional physiotherapy in that it understands the body to be a functionally integrated entity, inferring that constriction in one part of the body influences the entire body [34]. A key idea is that unresolved and difficult feelings, as well as continuing and high levels of life stress, are reflected in the body, including in the ANS, which is significant in this context as it relays experiences of stress to the respiratory system typically resulting in constricted breathing [35]. By the use of massage, stretching and grounding exercises, the aim is to release bodily tension and restricted breathing to increase bodily flexibility and stability, and to help patients tune into the body and understand that stressful experiences, relations and feelings are also bodily. The observing of respiration and changes in its patterns, rhythm and depth, is essential to NPMP. It is assumed that restricted breathing over time will affect the mechanisms of breathing, bodily expressions, functions and movements negatively [36, 37]. A key aim is typically a free and diaphragmatic breathing that moves through the thorax without restrictions. A breathing that is free does not require much thinking since it is controlled by the ANS.
Accordingly, the focus of the physiotherapy was not merely on improving the participants breathing as such, it also addressed bodily dealignments and bodily constraints, as these over time, can affect the function of breathing negatively. The physiotherapy was tailored to each individual participant according to their specific bodily restrictions related to respiration, posture, muscle tension and function. These features closely interact with one another. The restoration of the breathing was approached through careful release over time such that participants could integrate potential changes in their daily breathing. Several NPMP measures and practices were applied to facilitate and enable diaphragmatic respiration, including these:
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A balanced standing position, where the body is aligned and neck and shoulders are in a neutral position.
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A careful pressure and/or vibrations on the middle thoracic cage during the expiratory phase.
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Careful movement and retraction of larynx by the therapist.
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Massaging and stretching muscles directly related to, or assisting in, the breathing, such as muscles of the upper chest and neck.
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Massage and/or stretching of tense muscles in other body parts.
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Expiratory pursed lip practices can incite diaphragmatic breathing.
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Enacting a prolonged sigh through the mouth during the expiratory phase, where the mouth and jaws are relaxed, and wait for a “respiratory response”, was practiced and repeated in each consultation with the participants. The procedure may be labelled the “expiratory breathing practice” or “relaxed breathing out practice” (R-BOP). We prefer using “practice” to avoid an unfortunate focus on performing a right “technique”. R-BOP may be accompanied by holding one or both hands on the upper abdomen, just below the sternum, and wait for motion in the abdomen that accompany diaphragmatic inspiration.
B: Elements of cognitive-behavioural therapy
Cognitive behavioural therapy (CBT) involves a number of talking approaches and techniques adressing thoughts, emotions and behavior. It is commonly used to treat mild to moderate anxiety and depression, but is also useful for other mental and physical health issues. Key features of CBT are its focus on identifying and understanding existing ways of thinking and behaving, and on equipping people with tools to change their cognitive and behavioral patterns [38].
In this study, during the physiotherapy consultations with the participants, their thoughts and behaviour about training and competing were in particular addressed. To avoid respiratory symptoms and improve breathing during training and competition, the participants were provided with measures, such as holding one or two hands on the abdomen to cheque that the breathing movement was downwards, or diaphragmatic, as opposed to an upward movement taking place in the upper chest. This should be chequed out before the activity started and before further increase of intensity. The ultimate aim was to ensure a breathing that did not trigger EILO symptoms and to find a way that worked for the individual, in which she or he felt to be more in control of her/his breathing. One way to acquire such breathing was initially during low intensity training. Also, it was essential that the participants were aware of the position of the neck and kept the neck in a neutral position, since this is the ideal position for the airflow and laryngeal movements.
In addition, to lower the pressure and expectation about producing top results, which is a potential stressor that frequently trigger an upwards breathing movement (i.e., thoracic breathing), the participants were advised not to focus on results when they started to compete but rather on doing their sport technically well and think of it as a “routine training”. Lastly, to reduce overall stress and increase time and space for rest and restitution, the participants were encouraged to identify situations and activities (e.g., social media) in their daily life could be altered in terms of their level of involvement.
C: Rehabilitation plan
An individually tailored rehabilitation plan is required for the rehabilitation process of athletes recovering from acute injuries or chronic overuse of musculoskeletal structures and/or functions. Such a plan needs to take into account that a frequent goal of the person is to return to the same activity as before the injury occurred or the overuse materialized [39]. Since EILO primarily occurs during high-intensity exercise, usually lasts for months to years, and is often associated with thoracic breathing involving compensatory changes (e.g., increased activation of respiratory muscles and postural dealignments of the neck and shoulders) [40], it appeared appropriate to approach rehabilitation within the principles of a long-lasting overuse condition.
The rehabilitation plan for the participants in this study had a functional take and involved activities and exercises required for the athletes to return to their specific sports. Limiting further impairments and maintaining aerobic capacity without intensifying the EILO condition were key to the rehabilitation. The rehabilitation plan was individually tailored, but commonly included these three phases:
Phase 1 (week 1 – 6)
During the first intervention phase the participants were instructed to avoid activities that could lead to thoracic breathing which would stress respiratory muscles and laryngeal structures. The primary focus of the training was to take part in exercises with low intensity, while at the same time ensuring a diaphragmatic breathing.
Low intensity training implied that the participants could participate in large parts of their usual training activities, such as technique and strategic features where aerobic intensity is usually low. To help arrive at a diaphragmatic breathing, the participants were encouraged to use the R-BOP procedure (as described in the physiotherapy intervention), before and during natural pauses of the training. At the same time, postural alignment issues were addressed. For instance, given that the ideal position of the cervical spine for laryngeal movements is a neutral position, participants were encouraged to focus on keeping the shoulders in a lower position and the neck in a neutral position. Lastly, good warm up to ensure diaphragmatic breathing and stretching tight muscles were emphasized in all phases.
Phase 2 (week 7 – 12)
As tension in the laryngeal area and in respiratory muscles decreased and the breathing became more diaphragmatic both at rest and during training, the participants were advised to gradually increase the intensity of training to moderate aerobic training intensities (e.g., 72–87% of HRmax). It was still important to avoid activities and intensities that would trigger high costal breathing. The possibility of using the R-BOP was emphasized throughout the remaining phases to ensure a diaphragmatic breathing before all activities, but also during daily life activities.
Phase 3 (week 13 – 20)
As a diaphragmatic breathing pattern became more regular, the participants could gradually perform higher intensity training (e.g., 87–100% of HRmax) and begin competing in their respective sports. The basic goal for taking part in competitions was that the body functioned and breathing was diaphragmatic, rather than focusing on achieving top results or playing whole matches. Team athletes could, for instance, play parts of the game to ensure a functional breathing and feeling in control of the breathing before playing whole games. This was also a period when diaphragmatic breathing became more stabilized, a continuing process.
Statistics
Descriptive data are provided as median and interquartile range for continuous variables and counts for categorical variables. Continuous variables were normally distributed and a paired sample t-test with Bonferroni correction was performed for assessment of changes in physiological variables and in self-reported symptoms from pre to post intervention. In addition, we checked the results with a non-parametric test and the analysis showed almost equal p-values for the variables in Tables 2 and 3. Results are expressed as mean values with 95% confidence intervals (CI). P-values ≤ 0.05 were considered statistically significant.
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