Interaction of panic and episodic breathlessness among patients with life-limiting diseases: a cross-sectional study

Introduction

Chronic breathlessness is a common symptom in advanced life-limiting diseases (1). It occurs despite optimal treatment of the underlying disease and has a substantial impact on the functional status and the quality of life of patients (2,3). Studies showed that chronic breathlessness may lead to hopelessness, anxiety, and fear of death (3-5). Chronic breathlessness can be either continuous or episodic (6-9). Episodic breathlessness is “characterized by a severe worsening of breathlessness intensity or unpleasantness beyond usual fluctuations in the patient’s perception. Episodes are time-limited (seconds to hours) and occur intermittently, with or without underlying continuous breathlessness (…).” (10). Breathlessness episodes can occur daily, with variable frequency, are often severe and of short duration (median <5 minutes) (11,12). An American Thoracic Society workshop described that a dyspnea crisis, which can be considered as a longer-lasting form of a breathlessness episode (13), “overwhelms the patient and caregivers’ ability to achieve symptom relief” (14). The latter definition highlights the importance of the emotional component of breathlessness episodes (14). Chronic breathlessness is often accompanied by psychological symptoms such as fear, depression, anxiety or panic (15) and focus group interviews revealed panic attacks as one of the most common psychological symptoms among patients with chronic obstructive pulmonary disease (COPD) (16). The prevalence of panic attacks among COPD patients suffering from breathlessness varies between 8% and 67% (17) and is estimated to be around 10 times higher than in the general population (18). The co-occurrence of panic attacks in breathless patients leads to more hospital admissions and longer stays (19), greater disability and impaired functional status and quality of life (20). Conversely, it has been found that a large majority of people who suffer from panic attacks experience symptoms of breathlessness (21). The dyspnea-anxiety-dyspnea cycle (22) describes the close connection between breathlessness and anxiety. Episodic breathlessness, characterized by its short duration and a sharp increase in intensity, seems to interact even more closely with panic. It remains unclear if patients refer to panic attacks or episodic breathlessness when describing the phenomenon. As qualitative studies indicate, anxiety/panic triggers breathless episodes (10), and panic might be a consequence of a breathlessness episode (23). This can lead to a vicious cycle of escalating panic as patients with breathing difficulties describe (24). Patients who have once experienced the escalating feeling of panic in a breathlessness episode are afraid to be trapped in this vicious cycle again (23). Although there is valuable research on patients’ experiences with panic and breathlessness, as well as on the treatments available (16,25), such as cognitive behavioural therapy (26-28), the intersection between panic and episodic breathlessness, as well as the underlying mechanisms are unknown. Research on chronic breathlessness has shown that anxiety sensitivity and catastrophizing thoughts each predict panic symptoms (29), but research focusing on the interaction and possible predictors for panic in episodic breathlessness is still missing. Given the high burden patients with episodic breathlessness experience, especially caused by panic, a deeper understanding of the interaction between panic and episodic breathlessness is needed to develop appropriate and effective management strategies for these patients. Therefore, the present study aimed to describe and explore the interaction between panic and episodic breathlessness in patients suffering from life-limiting diseases to build a solid basis for the development of future treatment options. We present this article in accordance with the STROBE reporting checklist (available at https://apm.amegroups.com/article/view/10.21037/apm-22-1304/rc).

Methods

Participants

The patients of the cross-sectional study were enrolled for a single-arm phase II study evaluating a brief cognitive and behavioral intervention for the management of episodic breathlessness (CoBeMEB), conducted at the Department of Palliative Medicine, University of Cologne, Faculty of Medicine and University Hospital, Cologne, Germany (30). The data presented here were collected within the assessment of the phase II study. Suffering from episodic breathlessness due to any life-limiting and progressive disease despite optimal treatment of the underlying condition was the main inclusion criteria for participation. Further inclusion criteria were an estimated life expectancy of at least eight weeks, being older than 18, and being fluent in German. More information on recruitment and study procedure is reported elsewhere (30). The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). Ethical approval was provided by the Ethics Committee of University of Cologne (12/2018; No. 18-209) and all participants gave written informed consent. The project was registered with ClinicalTrials.gov (NCT04630743).

Study procedure

The assessments took place at the patients’ current place of residence. Self-report questionnaires and closed-ended questions about the interaction of episodic breathlessness and panic, as well as demographic and clinical data were administered during the baseline assessment of the phase II study. Six weeks later, an open-ended question on the interaction of panic and episodic breathlessness was asked.

Measures

Patients’ demographic and clinical data were assessed. They rated the average breathlessness intensity over the last 24 hours of a breathlessness episode, and the impairment due to an episode [numeric rating scales (NRS), 0 (no breathlessness/impairment) to 10 (worst breathlessness/impairment)] (31). They described the frequency and duration of the episodes. The Patient Health Questionnaire (PHQ) is a self-report inventory that is used as a screening tool for several mental health disorders (32). In our study, we used the panic module of the PHQ, which allows a tentative diagnosis of a panic disorder (“panic syndrome”). The Structured Clinical Interview for DSM-IV Diagnoses (SCID, conducted by trained professionals) is a semi-structured interview guide for making diagnoses according to the diagnostic criteria published in the DSM-IV (33). In our study, we used the anxiety section of the SCID, the diagnostic gold standard instrument for anxiety disorders (“panic disorder” or other anxiety disorders). To provide data for the exploratory data analysis, the following measures were used: The Breathlessness-Catastrophising-Scale assessed anxious beliefs related to breathlessness with 13 questions (BCS) (34). The Anxiety-Sensitivity-Index-3 (ASI-3) is a validated questionnaire for assessing anxiety sensitivity (35). All applied questionnaires have satisfying psychometric properties and were used in their German versions (32-36). Self-developed questions aimed to capture the panic experienced during a breathlessness episode, and a further question assessed how panic patients considered themselves in general (0 =no panic at all, 10 =extreme panic, please see Appendix 1). Patients were asked to complete the symptom checklist of the panic disorder section of the SCID (35) concerning the symptoms they experienced in a situation, in which they felt panic versus the experience of panic in a breathlessness episode.

Using an open-ended question, patients were asked to describe the experience of panic when suffering from a breathlessness episode (please think of the feeling of anxiety or panic in a breathlessness episode; please describe how this feeling manifests itself and what role it plays in this situation).

Statistical analysis

The anxiety section of the SCID was analyzed by two independent reviewers, and deviations in diagnosis were discussed until a consensus was reached. Exploratory statistical analysis was done using SPSS Statistics 26 (IBM Corp., Armonk, NY, USA). Descriptive statistics (mean, standard deviation, percentages, frequencies) and Pearson correlation coefficients were calculated. For group comparisons, the Wilcoxon rank-sum test or χ²/Fisher’s exact test was done, respectively with the α-level =0.05 (without multiplicity adjustment). High/low scorer groups were built following recommendations from the literature for the BCS (33,37) and ASI (38), and dichotomous variables (e.g., PHQ) were used for grouping the patients before testing for significant differences between them. Mediation analysis was used to test the influence of ASI and BCS on the relationship between the intensity of a breathlessness episode and experienced panic during an episode.

Content analysis was applied for analyzing qualitative data from the open-ended question (39). Answers were audio-taped, transcribed, and pseudonymized for analysis with MAXQDA (2020/2022). The main aspects of the patients’ experiences were summarized into the main categories panic, episodic breathlessness, and episodic breathlessness and panic. Further categories were inductively formed from the data material. Codings were discussed, revised, and finalized by the researchers.

Results

Patients’ sociodemographics and clinical data

Ninety-three eligible patients were invited to participate in the phase II study, 46 (49%) of them underwent the baseline assessment, 22 answered the open-ended question and 20 were interviewed by using the SCID. The majority of the patients suffered from COPD and they were balanced in terms of gender. The mean age was 66 years [standard deviation (SD) 7.3; Table 1]. Most patients described their breathlessness episodes as short (33/45; 73%: 1–10 minutes), intense [mean (M) =7.0; SD 2.1], and frequent (19/45; 42%: 1–3 episodes per day). They rated the mean impairment as 8.3 (SD 1.5) and the average intensity of breathlessness during the last 24 hours as 5.4 (SD 2.4). Triggers were asked using a multiple-choice question. The most frequently selected were exertion (n=41) and emotions (n=23). For further details on patients’ sociodemographics and clinical data, we refer to the corresponding paper (27).

Patients’ panic-spectrum pathology

The PHQ, administered at the baseline assessment, detected among 11/43 (26%) of the participants the presence of a panic syndrome. Five out of twenty patients (25%) were diagnosed with panic disorder and 2/20 (10%) with agoraphobia according to the SCID. Patients rated their feeling of being panic in general as low (M =3.38; SD 2.7).

Description of the panic experience in breathlessness episodes

Patients rated the panic experienced during a breathlessness episode as M =6.85 (SD 3.1). The presence of panic during a breathlessness episode varied: 14/41 (34%) patients experienced panic only at the beginning of an episode, 25/41 (61%) suffered from panic during the whole episode, and two patients (2/41; 5%) did not feel panic at any point during any breathlessness episode. Sixteen patients (16/41; 39%) always suffered from panic when having a breathlessness episode. See Table 2 for the patients’ ratings of episodic breathlessness and perceived panic during a breathlessness episode.

Experiencing panic in a general context, i.e., outside of episodic breathlessness, correlated significantly with the rating of panic intensity in a breathlessness episode (r=0.527; P≤0.001). Group comparisons using the Wilcoxon rank-sum test showed that patients with a panic syndrome experienced significantly more panic in a breathlessness episode than those without this syndrome (z=−1.96; P=0.047). There was no association between the presence of a panic syndrome and the frequency (F=2.57; P=0.501), duration (F=5.37; P=0.321), and intensity (z=−0.91; P=0.365) of the patients’ breathlessness episodes. The predictability of breathlessness episodes did not impact the frequency of panic in breathlessness episodes (z=−0.32; P=0.752) and patients who reported suffering from unpredictable breathlessness episodes did not suffer from unpredictable panic attacks (χ²₁=0.03; P=1.000).

The different patterns of panic associated with episodic breathlessness reflected by the quantitative data were also reported in the open-ended question. Patients’ descriptions of the interaction of panic and episodic breathlessness can be summarized in three main categories: (I) episodic breathlessness interacts with panic, leading to great fear and despair; (II) episodes that are not accompanied by panic; (III) the occurrence of panic alone, with no direct apparent association with a breathlessness episode. Two themes were generated inductively from the material: firstly, some patients described that they managed to differentiate episodic breathlessness from panic, and described the situations, in which breathlessness occurred with or without panic; secondly, some patients had developed strategies to avoid panic in a breathlessness episode. See Figure 1 for an overview of the categories (inductive/deductive) and Table 3 for categories and sample quotations.

Figure 1 Categories summarizing the patients’ experiences of panic and episodic breathlessness.

When experiencing panic during a breathlessness episode, patients suffered from significantly different symptoms compared to the symptoms they experienced when feeling panic in a different context. When describing panic outside of episodic breathlessness, the patients described more often palpitations (χ²₁=14.19, P≤0.001), trembling (χ²₁=7.93, P=0.013), sweating (χ²₁=9.21, P=0.008), a feeling of losing control (χ²₁=6.47, P=0.037), and nausea (χ²₁=33.70, P≤0.001). During a breathlessness episode accompanied by panic, they experienced more dry mouth (χ²₁=10.44, P=0.004), fear of imminent dying (χ²₁=11.98, P=0.003), and chest pain (χ²₁=11.34, P=0.004). Derealization, trepidation, dizziness, and breathlessness did not differ between both situations (P>0.05, Figure 2).

Figure 2 Comparison of symptoms the patients experienced during a breathlessness episode or in a different context. Asterisks indicate statistical significant differences (P<0.05) between the symptom frequency during an episode and a different situation.

Impact of catastrophizing thoughts and anxiety sensitivity on the experience of panic in episodic breathlessness

Those patients with high scores in the BCS (cut-off: ≥30) experienced more panic in a breathlessness episode (z=−3.49; P<0.001) and considered themselves to be more panic (z=−2.25; P=0.024) than those with low scores. There was a positive correlation between patients’ scores in catastrophizing thoughts and the episodes’ intensity (r=0.35; P=0.023). Mediation analyses showed a significant indirect effect of the intensity of episodic breathlessness on the panic experienced in an episode through catastrophizing thoughts regarding breathlessness (b=0.164; 95% CI: 0.105, 0.222). High anxiety sensitive patients (ASI, cut-off: ≥23) scored significantly higher in breathlessness catastrophizing thoughts than low anxiety sensitive patients (z=−2.98; P=0.003). Moreover, patients scoring high in anxiety sensitivity experienced more often unpredictable breathlessness episodes (z=−2.47; P=0.014; no further significant effects).

Discussion

The present study demonstrated that panic is highly present among patients with life-limiting diseases suffering from episodic breathlessness: most of the patients experienced panic at some point during an episode. The great majority of the patients differed in the frequency and duration of panic when suffering from a breathlessness episode. However, some patients did not always suffer from panic when being breathless that means that being breathless did not always lead to panic. Mechanisms for the absence or rapid reduction of panic needs to be further investigated. Panic-spectrum pathology influenced the feeling of panic in breathlessness episodes, and breathlessness catastrophizing thoughts played a major role in mediating the intensity of the episodes and the perceived panic during an episode. Patients developed strategies to avoid panic during an episodic breathlessness. These results are relevant for the development of appropriate support options to alleviate panic in episodic breathlessness among patients with life-limiting diseases.

Interaction of panic and episodic breathlessness

One-quarter of the patients suffered from a panic disorder or panic syndrome. Patients with a panic syndrome experienced more often panic in breathlessness episodes and the more panic patients were in general, the higher they rated the panic in an episode.

Both the quantitative and the qualitative data suggest a close association between episodic breathlessness and panic: patients indicated suffering from panic in most breathlessness episodes, but also described how they manage to avoid the rise of panic in some episodes. Most patients suffered from panic at some point during a breathlessness episode (at the beginning or during the whole episode) and in most of the episodes. Yet there was heterogeneity in the patterns of panic experience. Indeed, some patients described suffering from panic only, some from episodic breathlessness only and others from both episodic breathlessness and panic (attacks). The results showed that there are episodes, in which patients did not experience panic or managed to avoid it and that a very small minority never suffered from panic in such a situation. By investigating the interaction between panic and episodic breathlessness, four important patterns emerged: (I) most patients suffer from intense panic in an episode of breathlessness; (II) patients do not necessarily experience panic in a breathlessness episode and use strategies to avoid it; (III) suffering from panic or a panic syndrome in any context significantly interacts with panic experiences during breathlessness episodes; (IV) breathlessness catastrophizing thoughts are important in predicting panic in breathlessness episodes.

We also asked the patients to indicate which symptoms (e.g., trembling, palpitations) they experienced in relation to panic during a breathlessness episode as compared to symptoms related to panic outside the context breathlessness episodes. It was remarkable to note that for 8/11 symptoms, the frequency of occurrence differed significantly. Even though there is a statistically measurable difference in the symptom occurrence related to panic during and outside a breathlessness episode, the clinical experience shows that it is difficult to differentiate both forms of panic. It is important to know the origin of the panic in order to offer appropriate support.

Breathlessness catastrophizing thoughts

High-scorers in breathlessness catastrophizing thoughts felt more panic in a breathlessness episode and rated its intensity and unpleasantness higher than those with lower scores. Furthermore, catastrophizing thoughts about breathlessness mediated the interaction between the intensity of episodic breathlessness and the panic experienced during these episodes. This finding is important for tailoring support offers: research on non-pharmacological treatment options should focus on managing breathlessness-related catastrophizing thoughts to reduce the panic experienced in a breathlessness episode and thus the symptom burden. Findings on catastrophizing thoughts about breathlessness among patients suffering from chronic breathlessness underline the meaning of the breathlessness-related cognitions: patients with COPD and panic showed increased rates of catastrophic cognitions concerning bodily sensations (40), and catastrophic interpretations of breathlessness predicted panic-spectrum pathology in patients with COPD (39,41). Furthermore, patients who participated in the CoBeMEB trial (30) described in the open-ended question that they benefited from the intervention thanks to its impact on reducing panic during an episode (30). Next to the strategies implemented within the CoBeMEB intervention either as patient education (e.g., by addressing the triggers of breathlessness episodes) or as cognitive strategies focusing on anxiety control (e.g., distraction), the Breathing Thinking Functioning Model (BTF model) was used (27). The BTF model, and especially the thinking domain, focusses on the explanation (through pictures) of the close connection between emotions and (chronic) breathlessness, which can lead to escalating feelings of panic and breathlessness. This provides an opportunity to discuss patients’ fearful thoughts about their breathlessness episodes. The different strategies that are part of the intervention have in common that they might have positively affected the patients’ breathlessness-related catastrophizing thoughts, leading to the reported reduced feeling of panic. Given the CoBeMEB study design (feasibility study), this needs to be further evaluated. More importantly, as the present paper shows, working on the management of breathlessness catastrophizing thoughts could be an important tool to reduce panic in a breathlessness episode and thus the impairment caused by it.

Anxiety sensitivity

Anxiety sensitivity did not significantly mediate the interaction between panic and the intensity of a breathlessness episode. This is unexpected, as research among patients suffering from chronic breathlessness has identified anxiety sensitivity as a predictor of panic in this patient group (29). An explanation for the significance of the mediation of breathlessness catastrophizing thoughts but not for anxiety sensitivity is that breathlessness catastrophizing thoughts are more specific for the unique situation of breathlessness patients. While the assessment of a more general personal trait, that included social and cardiac subdomains unrelated to breathlessness, failed to mediate the interaction, the highly relevant cognition about breathlessness episodes yields significance. Group comparisons showed that patients scoring high in anxiety sensitivity suffer more often from unpredictable episodes than low scorers. Patients with panic disorder or respiratory diseases perceive even slight feelings of breathlessness as threatening as they may signal an impending catastrophe (e.g., critical somatic state/suffocation) (42). This might also be the explanation for the present findings: Patients who are very sensitive to bodily anxiety signs may pay more attention to physical signs. However, this may also lead them to interpret harmless signs as threatening, which can cause physical arousal leading to breathlessness.

Implications for research and clinical practice

The present study aimed to further understand the interaction between episodic breathlessness and panic to appropriately support patients. The experience of panic in breathlessness episodes varied between patients and even between the episodes of one patient. Yet two patients had never experienced panic when having a breathlessness episode. This needs to be further investigated, focusing on the factors that protect patients from experiencing panic or reduce the panic in a breathlessness episode. The present study succeeds to identify breathlessness catastrophizing thoughts as having a major influence on the interaction of episodic breathlessness and panic. Based on this, two implications arise: (I) research should focus on the psychological and emotional components that characterize the experience of episodic breathlessness; and (II) clinical practice should develop therapy options that focus on the management of breathlessness catastrophizing thoughts (e.g., cognitive-behavioral anxiety therapy) (43). Patients suffering from panic in breathlessness episodes could also benefit from the therapeutic concepts originating from anxiety therapy.

Strength and limitations

The present study is the first one to explore the interaction of episodic breathlessness and panic including interacting factors aiming to gain insights for the development of appropriate management options. Forty-six patients were included in the study and 22 participated in the interviews. This is a rather small but solid sample size. The difficulty to recruit vulnerable patients with a life-limiting disease for research purposes is a well-known challenge across the literature. However, this limitation could be mitigated thanks the open-ended question that complemented the quantitative results (44-46). While statistical analyses are limited due to the sample size, the qualitative data provided some insights into the patients’ individual experiences with panic and episodic breathlessness. However, they must be interpreted carefully as the open-ended question was presented after the cognitive and behavioural intervention (at week 6) which might have changed patient’s experience of panic and breathlessness. Quantitative data have been assessed at the beginning of the study ahead of the intervention.

For diagnosing the panic disorder, the SCID was used as a gold standard for diagnosing mental disorders. The diagnosed panic disorders need to be seen in the light of different limitations. As the SCIDs were applied within a single-arm phase II study (30), the SCID was conducted within the last appointment of the study procedure. The last appointment was chosen, to prevent any priming effect concerning the brief cognitive and behavioral intervention. But this includes the potential risk that the cognitive and behavioral intervention had an impact on the responses in the SCID, biasing the diagnosis. Furthermore, physical causes must be ruled out to assign the diagnosis of panic disorder. In the present sample, a physical cause (e.g., breathlessness episodes) cannot be excluded. For these reasons, the diagnosis of panic disorder can only be made with caution.

Conclusions

Patients suffering from episodic breathlessness often experience panic during these episodes, but the pattern varies between and within patients. Psychological components such as experiencing panic in a general context and cognitions about breathlessness play a major role in the interaction between panic and breathlessness episodes. Still, a very small minority never experienced panic during an episode. This underpins that further research on the mediating components, including factors protecting patients from feeling panic, is needed. As catastrophizing thoughts about breathlessness contribute to patients’ experiences of panic in episodic breathlessness, psychotherapeutic treatment might be promising in supporting patients to manage panic in episodic breathlessness. Research on appropriate management options for episodic breathlessness should not only focus on panic in breathlessness episodes but also on underlying mechanisms such as catastrophizing thoughts as they may maintain or aggravate the panic.

Acknowledgments

The study group would like to thank all participants for their time and interest. Summarized findings of the quantitative results was presented as a poster at the 12th World Research Congress of the European Association for Palliative Care 2022.

Funding: The work was supported by the Federal Ministery of Education and Research (No. 01GY1716 to Karlotta Schloesser, Anja Bergmann, Yvonne Eisenmann, Martin Hellmich, Max Oberste, and Steffen T. Simon). The funding source had no impact on the study design, on the data collection, analysis, and interpretation of the data nor on the writing of the report.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://apm.amegroups.com/article/view/10.21037/apm-22-1304/rc

Data Sharing Statement: Available at https://apm.amegroups.com/article/view/10.21037/apm-22-1304/dss

Peer Review File: Available at https://apm.amegroups.com/article/view/10.21037/apm-22-1304/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://apm.amegroups.com/article/view/10.21037/apm-22-1304/coif). KS, AB, YE, MH, MO, and STS report the funding from the Federal Ministry of Education and Research (No. 01GY1716). The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the local Research Ethics Committee of the University of Cologne (12/2018; No. 18-209) and informed consent was taken from all individual participants.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

References

1. Solano JP, Gomes B, Higginson IJ. A comparison of symptom prevalence in far advanced cancer, AIDS, heart disease, chronic obstructive pulmonary disease and renal disease. J Pain Symptom Manage 2006;31:58-69. [Crossref] [PubMed]
2. Currow DC, Abernethy AP, Allcroft P, et al. The need to research refractory breathlessness. Eur Respir J 2016;47:342-3. [Crossref] [PubMed]
3. Booth S, Silvester S, Todd C. Breathlessness in cancer and chronic obstructive pulmonary disease: using a qualitative approach to describe the experience of patients and carers. Palliat Support Care 2003;1:337-44. [Crossref] [PubMed]
4. Giacomini M, DeJean D, Simeonov D, et al. Experiences of living and dying with COPD: a systematic review and synthesis of the qualitative empirical literature. Ont Health Technol Assess Ser 2012;12:1-47. [PubMed]
5. Gysels M, Bausewein C, Higginson IJ. Experiences of breathlessness: a systematic review of the qualitative literature. Palliat Support Care 2007;5:281-302. [Crossref] [PubMed]
6. Reddy SK, Parsons HA, Elsayem A, et al. Characteristics and correlates of dyspnea in patients with advanced cancer. J Palliat Med 2009;12:29-36. [Crossref] [PubMed]
7. Simon ST, Bausewein C, Schildmann E, et al. Episodic breathlessness in patients with advanced disease: a systematic review. J Pain Symptom Manage 2013;45:561-78. [Crossref] [PubMed]
8. Simon ST, Higginson IJ, Benalia H, et al. Episodic and continuous breathlessness: a new categorization of breathlessness. J Pain Symptom Manage 2013;45:1019-29. [Crossref] [PubMed]
9. Simon ST, Higginson IJ, Benalia H, et al. Episodes of breathlessness: types and patterns - a qualitative study exploring experiences of patients with advanced diseases. Palliat Med 2013;27:524-32. [Crossref] [PubMed]
10. Simon ST, Weingärtner V, Higginson IJ, et al. Definition, categorization, and terminology of episodic breathlessness: consensus by an international Delphi survey. J Pain Symptom Manage 2014;47:828-38. [Crossref] [PubMed]
11. Weingärtner V, Bausewein C, Higginson IJ, et al. Characterizing episodic breathlessness in patients with advanced disease. J Palliat Med 2013;16:1275-9. [Crossref] [PubMed]
12. Weingärtner V, Scheve C, Gerdes V, et al. Characteristics of episodic breathlessness as reported by patients with advanced chronic obstructive pulmonary disease and lung cancer: Results of a descriptive cohort study. Palliat Med 2015;29:420-8. [Crossref] [PubMed]
13. Simon ST, Weingärtner V, Voltz R, et al. Episodic breathlessness: a clinically relevant and rising issue. Ann Am Thorac Soc 2014;11:274. [Crossref] [PubMed]
14. Mularski RA, Reinke LF, Carrieri-Kohlman V, et al. An official American Thoracic Society workshop report: assessment and palliative management of dyspnea crisis. Ann Am Thorac Soc 2013;10:S98-106. [Crossref] [PubMed]
15. Hallas C, Howard C, Wray J. Understanding panic disorder in chronic respiratory disease. Br J Nurs 2009;18:527-9. [Crossref] [PubMed]
16. Jarab A, Alefishat E, Mukattash T, et al. Patients’ perspective of the impact of COPD on quality of life: a focus group study for patients with COPD. Int J Clin Pharm 2018;40:573-9. [Crossref] [PubMed]
17. Hynninen KM, Breitve MH, Wiborg AB, et al. Psychological characteristics of patients with chronic obstructive pulmonary disease: a review. J Psychosom Res 2005;59:429-43. [Crossref] [PubMed]
18. Brenes GA. Anxiety and chronic obstructive pulmonary disease: prevalence, impact, and treatment. Psychosom Med 2003;65:963-70. [Crossref] [PubMed]
19. Gudmundsson G, Gislason T, Janson C, et al. Risk factors for rehospitalisation in COPD: role of health status, anxiety and depression. Eur Respir J 2005;26:414-9. [Crossref] [PubMed]
20. Kim HF, Kunik ME, Molinari VA, et al. Functional impairment in COPD patients: the impact of anxiety and depression. Psychosomatics 2000;41:465-71. [Crossref] [PubMed]
21. Anderson B, Ley R. Dyspnea during panic attacks. An Internet survey of incidences of changes in breathing. Behav Modif 2001;25:546-54. [Crossref] [PubMed]
22. Bailey PH. The dyspnea-anxiety-dyspnea cycle--COPD patients’ stories of breathlessness: “It’s scary /when you can’t breathe”. Qual Health Res 2004;14:760-78. [Crossref] [PubMed]
23. Linde P, Hanke G, Voltz R, et al. Unpredictable episodic breathlessness in patients with advanced chronic obstructive pulmonary disease and lung cancer: a qualitative study. Support Care Cancer 2018;26:1097-104. [Crossref] [PubMed]
24. Spathis A, Booth S, Moffat C, et al. The Breathing, Thinking, Functioning clinical model: a proposal to facilitate evidence-based breathlessness management in chronic respiratory disease. NPJ Prim Care Respir Med 2017;27:27. [Crossref] [PubMed]
25. Howard C, Dupont S. ‘The COPD breathlessness manual’: a randomised controlled trial to test a cognitive-behavioural manual versus information booklets on health service use, mood and health status, in patients with chronic obstructive pulmonary disease. NPJ Prim Care Respir Med 2014;24:14076. [Crossref] [PubMed]
26. Heslop-Marshall K, Baker C, Carrick-Sen D, et al. Randomised controlled trial of cognitive behavioural therapy in COPD. ERJ Open Res 2018;4:00094-2018. [Crossref] [PubMed]
27. Livermore N, Dimitri A, Sharpe L, et al. Cognitive behaviour therapy reduces dyspnoea ratings in patients with chronic obstructive pulmonary disease (COPD). Respir Physiol Neurobiol 2015;216:35-42. [Crossref] [PubMed]
28. Livermore N, Sharpe L, McKenzie D. Prevention of panic attacks and panic disorder in COPD. Eur Respir J 2010;35:557-63. [Crossref] [PubMed]
29. Livermore N, Sharpe L, McKenzie D. Catastrophic interpretations and anxiety sensitivity as predictors of panic-spectrum psychopathology in chronic obstructive pulmonary disease. J Psychosom Res 2012;72:388-92. [Crossref] [PubMed]
30. Schloesser K, Bergmann A, Eisenmann Y, et al. “Only I know now, of course, how to deal with it, or better to deal with it”: A mixed methods phase II study of a cognitive and behavioral intervention for the management of episodic breathlessness. J Pain Symptom Manage 2022;63:758-68. [Crossref] [PubMed]
31. Gift AG, Narsavage G. Validity of the numeric rating scale as a measure of dyspnea. Am J Crit Care 1998;7:200-4. [Crossref] [PubMed]
32. Gesundheitsfragebogen für Patienten (PHQ-D). Komplettversion mit vorläufigem Manual, Fragebogen, Schablonen; 2001.
33. Wittchen HU, Zaudig M, Fydrich T: SKID. Strukturiertes Klinisches Interview für DSM-IV. Göttingen: Hogrefe; 1997.
34. Solomon BK, Wilson KG, Henderson PR, et al. A Breathlessness Catastrophizing Scale for chronic obstructive pulmonary disease. J Psychosom Res 2015;79:62-8. [Crossref] [PubMed]
35. Psychometric properties of the German version of the Anxiety Sensitivity Index 3; 2009. Available online: URL: https://scholar.google.de/citations?user=qdztuguaaaaj&hl=de&oi=sra
36. Jerusalem M, Schwarzer R. SWE - Skala zur Allgemeinen Selbstwirksamkeitserwartung; 2003.
37. Sullivan MJL, Bishop SR, Pivik J. The Pain Catastrophizing Scale: Development and validation. Psychological Assessment 1995;7:524-32. [Crossref]
38. Allan NP, Raines AM, Capron DW, et al. Identification of anxiety sensitivity classes and clinical cut-scores in a sample of adult smokers: results from a factor mixture model. J Anxiety Disord 2014;28:696-703. [Crossref] [PubMed]
39. Ritchie J, Lewis J, Nicholls CM, et al. Qualitative Research Practice: A Guide for Social Science Students and Researchers. SAGE 2013;
40. Porzelius J, Vest M, Nochomovitz M. Respiratory function, cognitions, and panic in chronic obstructive pulmonary patients. Behav Res Ther 1992;30:75-7. [Crossref] [PubMed]
41. Giardino ND, Curtis JL, Abelson JL, et al. The impact of panic disorder on interoception and dyspnea reports in chronic obstructive pulmonary disease. Biol Psychol 2010;84:142-6. [Crossref] [PubMed]
42. Bouton ME, Mineka S, Barlow DH. A modern learning theory perspective on the etiology of panic disorder. Psychol Rev 2001;108:4-32. [Crossref] [PubMed]
43. What Is Cognitive Behavioral Therapy? In: Joyce-Beaulieu D, Sulkowski ML, editors. Cognitive behavioral therapy in K-12 school settings: A practitioner’s toolkit. New York, NY: Springer Publishing Company LLC; 2015 [cited 2023 Mar 10]. Available online: https://www.apa.org/ptsd-guideline/patients-and-families/cognitive-behavioral.pdf
44. Blum D, Inauen R, Binswanger J, et al. Barriers to research in palliative care: a systematic literature review. Prog Palliat Care 2015;23:75-84. [Crossref]
45. Bullen T, Maher K, Rosenberg JP, et al. Establishing research in a palliative care clinical setting: perceived barriers and implemented strategies. Appl Nurs Res 2014;27:78-83. [Crossref] [PubMed]
46. Kars MC, van Thiel GJ, van der Graaf R, et al. A systematic review of reasons for gatekeeping in palliative care research. Palliat Med 2016;30:533-48. [Crossref] [PubMed]