Support Care Cancer https://doi.org/10.1007/s00520-017-3928-9

ORIGINAL ARTICLE

Unpredictable episodic breathlessness in patients with advanced chronic obstructive pulmonary disease and lung cancer: a qualitative study P. Linde 1,2 & G. Hanke 1,2 & R. Voltz 1,2 & S. T. Simon 1,2

Received: 10 May 2017 / Accepted: 9 October 2017 # Springer-Verlag GmbH Germany 2017

Abstract Purpose The internationally consented definition and categorization describe two categories of episodic breathlessness: predictable (with known triggers) and unpredictable. The link of known triggers only to predictable episodes can be read that unpredictable episodes have none known trigger. Our aim was to illuminate patients’ experiences with episodes of unpredictable breathlessness, to collect descriptions of the episodes’ impact on the patients’ lives, and, in turn, the patients’ individual coping strategies in this connection. Design Qualitative study using semi-structured in-depth interviews with patients suffering from unpredictable episodes of breathlessness and chronic obstructive pulmonary disease (COPD; Global Initiative for Obstructive Lung Disease III and IV) or lung cancer (all stages). Interviews were audiorecorded, transcribed verbatim, and analyzed using Framework Analysis. Results One hundred one patients were screened in a large university hospital; ten participants fulfilled the inclusion criteria and provided consent. The experienced episodes were evaluated as unpleasant and with higher intensity compared to predictable episodes. Non-pharmacological interventions were identified as useful coping strategies. Interestingly, although patients experienced the episodes in an unpredictable

* S. T. Simon [email protected] P. Linde [email protected] 1

Department of Palliative Medicine, University Hospital of Cologne, Kerpener Str. 62, 50937 Cologne, Germany

2

Center of Integrated Oncology (CIO) Cologne/Bonn, University Hospital of Cologne, 50937 Cologne, Germany

manner, a trigger could be detected retrospectively for the majority of cases (mostly emotions (especially panic) and, occasionally, physical exertion). Unpredictable episodes are less frequent than previously assumed. Conclusion The unpredictability of unpredictable breathless episodes refers to the patients’ experience that these episodes occur Bout-of-the-blue.^ However, a known trigger can be identified for the majority of unpredictable breathless episodes. These are therefore triggered as well. Further research needs to describe more possible triggers, to inquire the prevalence of unpredictable episodic breathlessness, and to develop effective management strategies. Keywords Episodic breathlessness . Coping . Palliativecare . Chronic obstructive pulmonary disease . Lung cancer

Introduction Chronic obstructive pulmonary disease (COPD) and lung cancer (LC) are common life-threatening lung-diseases that often have adverse effects on the ability to breathe [1]. In 2012, more than 4.59 million people died of COPD and LC worldwide; the diseases are already expected to be leading causes of death worldwide by 2030 [1, 2]. In advanced stages, up to 81% of patients suffer from episodic breathlessness, one form of refractory breathlessness that persists despite optimal treatment of the underlying disease [3, 4]. Episodic breathlessness is Bcharacterized 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. Episodes may be predictable or unpredictable, depending on whether any trigger(s) can be identified (…)^ [5].

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Unpredictable episodes of breathlessness have rarely been described before. What we know from descriptive studies is that breathless episodes are often short in duration (median of 5 min), high in intensity (mean of 6/10 NRS), and occur regularly (daily) [4, 6]. As found in a qualitative study of our group with 51 patients in 2010, nearly half of these patients experienced attack-like episodes of breathlessness, occurring out-of-the-blue and—therefore—unpredictably [7]. Based on this qualitative study together with other qualitative and quantitative descriptions, international experts consented a definition and categorization of episodic breathlessness in 2014 [5]. This definition categorizes episodic breathlessness in two types—predictable and unpredictable episodes—differentiated by the fact whether a trigger can be identified. However, it is unclear whether this link mirrors patient experiences and helps clinicians for a better understanding of patients’ individual experience of breathless episodes. Therefore, the aim of this study is to further explore and describe patients’ experiences of unpredictable episodes of breathlessness. We aimed to produce extended descriptions and insights to investigate the Bunpredictability,^ the impact of unpredictable episodic breathlessness on the patients’ lives, and their individual coping strategies Fig. 1.

Methods Study design and ethics We used a qualitative study design with semi-structured, faceto-face in-depth interviews. This study followed the consolidated criteria for reporting qualitative research (COREQ) [8]. Ethical approval was obtained from the Ethics Commission of the Faculty of Medicine of the University of Cologne (Reference Number 13-323).

Fig. 1 International definition of episodic breathlessness

collected by the interviews, we assumed saturation and stopped recruitment. Data collection Before the interviews started, the patients were informed about both the aim and the process of the study as well as a short personal description of the interviewer. Verbal and written informed consent was obtained from the participants at least 24 h before the interview. The face-to-face in-depth interviews were performed by one trained interviewer (PL (male, medical student, skilled by STS)) in the inpatient clinics. Each interview began with an open question asking the patients to describe an unpredictable episode of breathlessness of their choice. We encouraged patients to comprehensively think aloud and report about any topic they felt to be significant in the area of unpredictable episodes of breathlessness. A semi-structured interview guide was used in order to address all predefined notable topics: &

Participants and recruitment We used the internationally consented definition of episodic breathlessness [5]. Patients were eligible if they stated to experience unpredictable episodes of breathlessness due to LC (all stages) or COPD (stage III/IVof the Global Initiative for Obstructive Lung Disease (GOLD) classification). In order for an interview to be able to be analyzed, the three questions in Table 1 needed to be affirmed. Participants could be on any treatment with regard to the primary disease or breathlessness, including surgery, radio-, or chemotherapy. Patients were excluded if they were not able to give informed consent or suffered from cognitive impairment (clinical judgment by the attending professionals). Recruitment of participants (convenience sampling) took place in three inpatient clinics of the University Hospital Cologne in 2014/15. When no new information could be

& & & & & &

general experience with unpredictable episodes of breathlessness, characteristics of unpredictable episodes of breathlessness, individual descriptions of the term Bunpredictable episodes of breathlessness,^ health care use, wishes and needs, prevention and management strategies, and impact on activities of daily living (ADL).

Demographic and clinical data were obtained as follows: age, gender, primary disease, smoking status, oxygen supply, modified Borg Scale, Karnofsky Index, Charlson Comorbidity Index, and Palliative care Outcome Scale Symptom list (POS-S) (see Table 2) [9–12]. Initially, the data was gathered before starting the interview. While interviewing the first three patients, the researcher noticed patient-related difficulties in answering the questions, e.g., the participants

Support Care Cancer Table 1 Inclusion criteria: enclosing questions

Question

Answer (yes/no)

Do you have experiences with breathlessness in general?

Yes

Have you ever had experiences with predictable episodes of breathlessness?

Yes/no

Have you ever had experiences with unpredictable episodes of breathlessness?

Yes

got tired reporting twice about unpredictable episodes of breathlessness. In further consequence, we decided to ascertain the data after the interview. Debriefing was offered after each interview to give support if needed. All interviews were audio-recorded and fully transcribed using verbatim transcription rules. The interviewer kept notes related to the interview and epiphenomenon after each interview in patient-related memos. Data analysis Descriptive analysis was conducted for demographic and clinical data of participants (percentage, mean, standard deviation, median, and range). The interviews were qualitatively analyzed using Framework Analysis (FWA). This is a matrixTable 2 Demographic and clinical characteristics of participants

based, systematic, and comprehensive approach using a thematic framework to manage and structure data by detecting themes, categories, and a theory [13]. FWA reduces data through summarization but always retains links to the original data. It combines thematic (look down) and case analysis (look across). FWA is structured in three hierarchic stages: data management (finding initial themes, coding), descriptive accounts (sorting, summarizing, identifying dimensions and categories), and explanatory accounts (detecting patterns, developing explanations, and building a theory). First, all interviews and memos were read multiple times to familiarize with the contents (PL). Three interviews were analyzed by two researchers (PL, STS) in order to address accuracy and dependability of the coding. Findings were interchanged regularly among the research team. The computer program

Characteristic

n = 10 (100%)

Age—mean (SD; range) Female Primary disease COPD LCr

57 (9; 40–74) 7 (70%)

Charlson Comorbidity Index—median (range) Karnofsky Index—median (range) Palliative Care Outcome Scale (POS-S) median (range) Non-smoker Oxygen supply COPD LCr Impairment of breathing in general, mod. Borga (scale 0–4), mean (SD) Average 72 h

3.5 (2–9) 60 (30–90) 15 (6–28) 4 (40%)

Intensity of breathlessness in general, mod. Borga (scale 0–10), mean (SD) Intensity of episodic breathlessness, mod. Borga (scale 0–10), mean (SD)

7 (1.3)

Discomfort during episodic breathlessness, mod. Borga (scale 0–10), mean (SD) Coping capability, mod. Borga (scale 0–10), mean (SD)

6 (60%; 1/5 GOLD III/IV) 4 (40%; 3/1 NSCLC/SCLC)

6 (60%; 1/5 GOLD III/IV) 2 (20%; 2 NSCLC) 2.1 (1.3)

8/8 (2.4/1.8) (unpredictable/predictable) 9/7 (2.5/3) (unpredictable/predictable) 5/7 (3.3/1.7) (unpredictable/predictable)

Numbers and percentages are presented unless otherwise stated COPD chronic obstructive pulmonary disease, GOLD Global Initiative for Chronic Obstructive Lung Disease, LCr lung cancer, SD standard deviation a

mod. Borg = modified Borg Scale, a numeric scale from 0 to 10 combined with verbal descriptors of severity from Bnot at all^ to Bmaximum^ [9]

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MAXQDA12 was used to support data management and analysis.

Results

Recreational activities of daily living [14] Most patients reported that unpredictable episodes of breathlessness could occur during any recreational activities of daily living (RADL) at any time. The RADL were described as not exhausting and the unpredictable episode of breathlessness as occurring outof-the-blue.

Participants Of 101 patients screened, 18 reported experiencing unpredictable episodic breathlessness. Eight of the 18 patients were in a progressed phase of illness and too weak to be interviewed; these statuses were either assessed by the patients themselves or the interviewer. Thereby, ten patients consented to take part in the study. The recruitment discovered a much lower prevalence of unpredictable episodic breathlessness than previously assumed (a result of the study) which led to 100% extension of the recruitment time. Six patients with COPD and four patients with lung cancer with a mean age of 57 years and seven female were interviewed. The interviews took place in the patients’ rooms and the median duration of the interviews was 56 min (range 48 to 68 min). During two interviews, other (nonparticipating) people were present (e.g., patients, husband). Categories Two main categories with subcategories emerged during the analysis process from the data.

I didn’t do anything special, I was watching (...) television, news, just what you do. Suddenly, it occurred. (LC-2) Then, so bad, quite terrible, a shortness of breath that comes out of nowhere. (COPD-1) Eight participants reported that unpredictable episodes of breathlessness could take place at night; one patient stated that the episodes happened exclusively at night. I wake up at night, because I am running out of air. (COPD-3)

Anxiety and panic The majority of participants (8/10) experienced anxiety as the underlying feeling during an unpredictable episode of breathlessness. In addition, panic was named as a reaction and state of intense anxiety by seven patients. Once experienced, all participants feared having a panic attack again.

Experience and descriptions of unpredictable episodic breathlessness Characteristics of unpredictable episodic breathlessness The experienced unpredictable episodes were evaluated as more unpleasant and stronger than those with known triggers; the participants stated worse capabilities to cope with those unpredictable episodes in contrast to generally better coping abilities on predictable ones. Unpredictable episodes of breathlessness occurred more rarely (several times per week) than predictable ones (up to several times a day). They occurred during day and night. Probing the causes of unpredictable episodes and asking the patients about their guess of a trigger, emotions like stress, e.g., brought on by disputes within the family, were often named and emerged therefore retrospectively as a trigger. Interestingly, the participants were able to describe potential triggers, but the arising of the episodes was always unpredictable. Furthermore, the episodes of unpredictable breathlessness occurred less often than reported earlier [7].

(…) thinking and pondering itself may provoke an attack, although unconsciously! (COPD-2)

(…) Panic attacks belong to it! (…) There is nothing worse! (…) You no longer know what to do! (…) I do not want that anymore – it is terrifying! (COPD-1) Fear of death by suffocation was the main cause of anxiety and panic. The participants said that these emotions had worsened their disability, limiting them even more. Facing the emotions was described as Bintense^ (COPD-1). Triggered by fear, I also remember that I said: ‘Dear God, help me!’ (COPD-1) Especially, panic and ruminating thoughts were mentioned right before an unpredictable episode of breathlessness. However, the episodes remain fundamentally unexpected for the patients. Frustration Frustration was a common emotional response according to unpredictable episodes of breathlessness. The patients felt isolated or restricted in their activities by the threat of unpredictable episodes of breathlessness. Furthermore, the inability to cope with unpredictable episodes of breathlessness

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was mentioned as quite distressing. One participant speculated that Bthinking negatively about an attack causes another^ (COPD-2) one.

Of course does it restrict you severely. You can’t behave as freely as you did before. (COPD-2)

Coping and management strategies of unpredictable episodic breathlessness Informed patient Each participant presented and named personal features to deal with unpredictable episodes of breathlessness like a strong will and assertiveness, but also to Brebel^ against unpredictable episodes. Patients who were fully informed about the advanced stage of their disease and aware of possible unpredictable episodes of breathlessness managed with unpredictable episodes much better. Conditions such as major depression found by one patient as an apparent co-morbidity made it more difficult for the patient to cope with upcoming episodes. One patient showed a profound acceptance of the stage of his illness and the appearance of unpredictable episodes of breathlessness.

I do not attach great importance to this. It is unpleasant, but (...). (LC-3) The participants stated a strong will to live and motivation to try new methods according to unpredictable episodes of breathlessness, too. Even the participation in the study gave a life-affirming effect to some of the patients, stated when bidding the interviewer farewell. However, some declared their will to live associated with Bhaving a better – or at least: not worse – quality of life^ (COPD-1). Cognitive and psychological strategies The participants reported to embark on their inner voice during an unpredictable episode of breathlessness. Thoughts like BCalm down.^ or BEverything is going to be fine.^ (LC-3) and assuring that nothing worse would happen. In addition, touching the flexible tube of the oxygen supply and listening to the sound of the O2-bubbles seemed to have a calming effect on the patients. Assessment of the severity of the unpredictable episodes of breathlessness is getting better during long-term illness and underlined by the patient-related intuition.

Because (…), you learn to assess them. With ‘small ones’, you can cope on your own. (COPD-5)

The knowledge of the fact that the breathless episode will stop and relaxing breathing will come back helps to calm down and cope. In addition, relaxation via meditation exercises and motivational thoughts during the unpredictable episodes of breathlessness were stated as helpful strategies to come through it. The participants reported that they have learned those techniques on their own (e.g., Jiu-Jitsu) or during pulmonary rehabilitation. I’ve calmed down — how should I say? I used to do martial arts and we had to calm down before the workout. So, it sounds a little bit strange: ‘Ommh’ and it worked. (LC-3)

Breathing techniques and positioning All participants used at least one breathing technique (e.g., pursed-lip breathing, abdominal breathing) and positioning (e.g., leaning forward) and described them as helpful for their coping—irrespective of their primary disease. Mentioned techniques were taught by health care professionals and fellow patients or appeared intuitionally. A through Jiu-Jitsu inspired breathing technique was also reported as helpful. Drugs and medical devices Participants reported several experiences with inhalers and intravenously injected steroids. However, steroids were unanimously reported by patients with advanced COPD as the most useful drug according to unpredictable episodes of breathlessness, Bbecause you feel immediately better when it shoots through the veins^ (COPD-4). Eight participants (six COPD, two LC) used permanent oxygen supply and described oxygen as very helpful in coping with unpredictable episodes of breathlessness. One patient (COPD-4) was equipped with a non-invasive continuous positive airway pressure mask. In the event of an unpredictable episode of breathlessness, he used it for 2 min but called the emergency doctor whenever he could not cope with the episode on his own. Inhalers (short-acting and long-acting types) also offered relief but were not described as significantly helpful. Medication as required (pro re nata) was not mentioned to be helpful in regard of upcoming episodes. One patient (COPD-2) reported that he does not take prescribed opioids (e.g., morphine) because of his fear to get addicted. Personal care Nine out of the ten patients said they benefitted from personal support during an unpredictable episode of breathlessness, and it was stated to be irrelevant whether family members or health care professionals gave support. This support included presence, soft touch, calming down via the present person, and the awareness that the other person can call for help.

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Yes, if someone is there, that is a difference. I know there is someone who can help me. (COPD-5) In contrast, one patient experienced the presence of another hectic person as debilitating. BI go into my room where it is quiet, (…), other people react hectically — I can’t calm myself down!^ (COPD-6). However, one participant reported that B(…) in the end, you have to stand it [unpredictable episodes of breathlessness] on your own!^ (COPD-4).

Discussion This is the first study focusing on patients’ experiences of unpredictable episodic breathlessness. Patients with advanced COPD and LC experience unpredictable episodic breathlessness as coming out-of-the-blue at any time. They perceived these episodes both as terrifying and restricting, and more severe than predictable episodes (see Table 2). Furthermore, patients find it more difficult to cope with unpredictable episodic breathlessness (ibid.). Breathing techniques and cognitive and behavioral interventions have been identified as useful coping strategies. The most important external resource during an episode is emotional support and presence by another person (relatives, medical staff). Interestingly, a known trigger can be identified for the majority of unpredictable breathless episodes which are therefore triggered as well. Consequently, the international definition of episodic breathlessness needs to be adapted, stating that both types of episodes (predictable and unpredictable) are mostly triggered by known triggers. Unpredictability and presence of known trigger The international consensus of episodic breathlessness differentiates between predictable and unpredictable episodes [5]. For predictable episodic breathlessness, four types of triggers have been described. The link of known triggers only to predictable episodes can be interpreted that unpredictable episodes might not have a trigger. Our data suggest that this need to be changed because participants reported triggers of the majority of unpredictable breathless episodes (predominately emotions—after making an enquiry more in depth). BUnpredictability^ is a subjective experience of surprise and emergency (out-of-the-blue). Some triggers seem to provoke episodic breathlessness but not every time, and patients cannot predict when the trigger will lead to a breathless episode. In only a few cases, the Bunpredictability^ remains diffuse and currently Bnot triggered^ at the moment. This might change with further exploration and assessment, including clinical and diagnostic measures in order to discover triggers for all episodes. Further evaluation is required.

Panic and episodic breathlessness It remains unclear whether panic has to be classified as a trigger or as a consequence of unpredictable breathlessness or both. Nevertheless, our assumptions regarding panic as a potential trigger of both—unpredictable and predictable—episodes of breathlessness and a panic-spectrum psychopathology (denoting panic attacks and panic disorder) are consistent with the work of Greer et al., Shin et al., Vögele and von Leupoldt, and Livermore et al. who described patients with severe COPD or LC [15–18]. Greer et al. delivered a brief behavioral intervention for breathlessness in patients with LC [15]. Hereby, improvements in breathlessness, quality of life, and mood were found. Shin et al. found that more than twice as many patients with newly diagnosed non-small cell lung cancer with breathlessness episodes show symptoms of panic disorder than patients without breathlessness [16]. Examining patients with advanced COPD, Vögele and von Leupoldt highlighted panic disorder as particularly common [17]. Livermore et al. detected cognitive behavior therapy (CBT) for patients with COPD suffering from panic attacks and panic disorder as potentially useful [18]. Their follow-up study then tested CBT in the group of patients and found a relevant decrease of 17% in ratings of breathlessness [19]. Management and coping strategies Patients reported a number of different steps to cope with unpredictable episodes of breathlessness and profited accordingly from various in- and external resources, which are—as the named strategies—easy to enforce, nearly anywhere at any time. According to previous work, primarily nonpharmacological strategies were pointed out as effective [20]. Spathis classified those non-pharmacological strategies into three groups: breathing, thinking, and functioning [21]. These data agree with our findings according to unpredictable episodes, where, in particular, cognitive and behavioral strategies referred to be practical. At this time, it seems that there are no differences in management and coping strategies of predictable and episodic breathlessness in general in comparison to unpredictable episodes. Implications for clinical practice and research Special services are needed, on the one hand, to empower the patients to use their self-taught and individualized strategies, on the other hand, to offer the strategies to other patients with advanced pulmonary disease. Developing guidelines, handing information leaflets to patients and their relatives, and teaching exercises in pulmonary rehabilitation are indispensable tasks for a multi-professional team to take on. Previous work

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by our group describes six main strategies that can be used as a quick, easy-to-integrate checklist for professionals, who work with pulmonary-constricted patients and their relatives, to detect potential triggers and to prevent episodic breathlessness [22, 23]. The development and evaluation of a comprehensive and practical intervention for predictable and unpredictable episodic breathlessness is under way using cognitive and behavioral strategies in order to support patients’ selfmanagement. Multi-professional cooperation concerning the therapeutic approach is needed, e.g., involving psychiatrists to diagnose and treat any existing anxiety disorder. Comparable to panic attacks, unpredictable episodes of breathlessness occur within seconds and often out of the blue. On the one hand, more research is necessary to better differentiate panic and breathlessness episodes. On the other hand, specifically targeted behavioral interventions may stop development or worsening of panic-spectrum psychopathology. Unpredictable breathless episodes are burdensome and terrifying. More research is needed to evaluate whether this differentiation (between predictable and unpredictable breathlessness) is relevant for the management of episodic breathlessness. Above all, it should not be forgotten, rather further examined, that triggers might be unconscious. Strengths and limitations The study sample was possibly lacking in diversity to the effect that the screened patients were either suffering from unpredictable episodes of breathlessness due to COPD (GOLD III and IV) or lung cancer (all stages). We used a qualitative, descriptive study and therefore further quantitative verification is necessary. However, the in-depth insights into the patients’ experiences and the named coping strategies point towards important aspects. The results provide hypotheses, particularly regarding a panic-based psychopathology explanation for the development of unpredictable episodes of breathlessness in patients with COPD and LC.

We thank the staff at the participating centers for their support on recruitment. Special thanks to Vera Weingärtner and Maren Piel for their professional advice. We would also like to thank Fabia Bertram for her support in proofreading as a native speaker. Compliance with ethical standards Informed consent was obtained from all individual participants included in the study. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Conflict of interest The authors declare that they have no conflicts of interest.

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Conclusion

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The unpredictability of unpredictable breathless episodes refers to the patients’ experience that these episodes occur Boutof-the-blue.^ However, a known trigger can be identified for the majority of unpredictable breathless episodes. These are therefore triggered as well. Further research needs to describe more possible triggers, to inquire the prevalence of unpredictable episodic breathlessness, and to develop effective management strategies.

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15. Acknowledgements The authors thank all participants of the study for their willingness to participate and give insights into their experiences.

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