Psychoeducational groups for people with Amyotrophic Lateral Sclerosis and their caregiver: a qualitative study

The current study aimed to describe the implementation of a structured psychoeducational intervention in Amyotrophic Lateral Sclerosis (ALS), identifying the needs of both patients and their caregivers. Five patients and thirteen caregivers attended eight psychoeducational group meetings at the Respiratory Rehabilitation Unit of IRCCS Santa Maria Nascente of Fondazione Don Carlo Gnocchi, Milan (Italy) and eight participants underwent semi-structured interviews once the group sessions ended. Group sessions and semi-structured interviews were audio-recorded and transcribed verbatim. Then, data obtained by group meetings’ transcripts have been analysed using the grounded theory (GT) paradigm, while those obtained by interviews have been analysed using the interpretative phenomenological analysis (IPA). The analysis of the meetings allowed us to identify seven main themes: “practical advice”, “explanation of the pathology”, “recognition of emotions”, “adaptation”, “family and relationships”, “being caregiver of oneself”, and “sharing”. Twenty-one sub-themes also emerged from the transcripts’ analysis. The analysis of the interviews allowed us to deduce the main reasons to participate (i.e., to have information and to be able to share experiences), the positive and negative aspects of the experiences. These results suggested the usefulness of psychoeducational groups in the regular clinical practise to allow patients and caregivers to share advice, emotions, and experiences with others in the same situation. This study displays the utility of psychoeducational group intervention in supporting people with ALS and their caregivers because of two main reasons: first for the psychoeducation provided by professionals; second for the possibility of sharing experiences and emotions with people in the same situation.


Introduction
Amyotrophic Lateral Sclerosis (ALS) is a neurodegenerative disease with unknown aetiology characterized by the progressive loss of lower and upper motor neurons [1,2]. There are currently no effective disease-modifying therapies, and management is symptomatic; death often occurs in 3 to 5 years from the onset [1,[3][4][5].
The diagnosis strongly impacts both patients' and caregivers' lives. Anxiety and depression are the most common psychopathological features of people with ALS, with an estimated prevalence of 30-70% for anxiety and 40-70% for depression [6][7][8]. In the daily experience of a progressive and gradual loss of functional and instrumental abilities, many of the existential autonomies and freedoms are eroded. For this reason, in addition to the more evident symptoms, patients with ALS tend to have some unconscious reactions among which, in particular, denial and splitting, which allow them not to be overwhelmed by the onset of intense emotions experienced as threatening [9,10].
Other psychologically significant reactions are resentment, thirst for compensation, hatred, emotional lability, loss of hope, and even suicidal ideation [11,12]. Although psychological and psychotherapeutic interventions are usually suggested to deal mainly with anxious or depressive symptoms, they become relevant, albeit with different connotations at different stages of the disease. However, there are no studies in the literature that give a clear picture of how and when it is best to address these issues in relation to the stages of the disease.
Care delivered by a multidisciplinary team has been shown to better address the complex needs of patients [13]. Informal caregivers play a fundamental role in ALS management, by taking most of the responsibility [14][15][16]. The burden of care is one of the most important psychological features of being an ALS patient's caregiver; anxiety and depression reactions are most common along caregivers, as well as an impairment of quality of life (QoL), which increase as the patient's disease progresses [14,[17][18][19].
Although psychological interventions are useful for reducing patient and caregiver anxiety and depression and for improving their QoL, there is still a lack of research on psychological treatments [20,21]. Gould et al. (2015) in their systematic review about psychotherapy for reducing distress and improving well-being in people with ALS found that there is no evidence to support the use of a specific psychotherapy intervention [21]. Bentley et al. (2014) found that dignity therapy, a brief psychotherapy aimed to promote hope and dignity and to reduce psychological distress, was feasible and acceptable for people with ALS, but they had no pre-test post-test significant changes for psychological distress [22]. Palmieri et al. (2012) demonstrated the feasibility of a hypnosis-based intervention and its efficacy to manage ALS physical symptomatology and to cope with ALS psychopathological implications [23]. In a later study, authors confirmed the feasibility of hypnosis-based treatment and the efficacy on physical and psychological symptoms; moreover, authors found that patients' results were indirectly associated with benefits in caregivers [24].
Recently, Palmieri et al. (2021) conducted a study on empathy-based supportive counselling treatment for people with ALS; the authors demonstrated the efficacy in improving patient well-being [25]. Although there is limited information on the efficacy of group interventions, previous studies suggest the potentially positive impact of group interventions in people facing chronic diseases [26][27][28][29][30]. Previous studies had analysed psychological group intervention, providing some information regarding coping strategies used by people facing ALS and their caregivers [31][32][33]. Madsen et al. (2018) analysed a group rehabilitation therapy for ALS people, detecting an increased understanding of the disease and a sense of community, which helps to fight together against ALS [33]. Additionally, Locock and Brown (2010) found that, by attending a support group, individuals gained both practical and social support and opportunities for social comparison [32]. The first study that analysed support group participation in Italy has been conducted by Cipolletta et al. (2018), showing that caregivers' experience is different for partners and children and who, importantly, had the opportunity to express feelings and experiences without being judged by others [31].
As stated by De Wit et al. (2020), a support intervention including psychoeducation, mindfulness exercises, and practical information could be helpful for family caregivers of people with ALS [34].
Despite the contributions illustrated above, there is a lack of studies that examined the impact of psychoeducational groups for people with ALS and their caregivers as well as the needs they can answer during this experience. Such theory-based studies may help facilitate standardized psychoeducational intervention efforts, tailored to the development of enhanced both psychological and quality of life outcomes.
The current study aimed to describe the implementation of a structured psychoeducational intervention in ALS, by identifying the needs of both patients and their caregivers. We report preliminary results on patients' and caregivers' perceptions of the psychoeducational intervention's relevance to their lives and satisfaction about their attendance.

Ethics statement
This study was conducted following the principles of the Helsinki Declaration and approved by the Ethics Committee of IRCCS Fondazione Don Carlo Gnocchi. All the participants were informed that the meetings would be audiorecorded. If they accepted, they were invited to read and sign in the consent form for data collection and pseudonyms were used to preserve their anonymity.

Participants
ALS patients and their informal caregivers attending the Respiratory Rehabilitation Unit of IRCCS Santa Maria Nascente of Fondazione Don Carlo Gnocchi, Milan (Italy) and the related outpatient clinic accesses were recruited between June and November 2018.
They were approached by a research assistant (VAB) and provided with information about the research study. The psychoeducational program was advertised within the Unit and during the clinical appointments through verbal invitations, email, and printed flyers. Psychologists evaluated if there were the emotional and cognitive conditions to take part in the study, as well as if the inclusion criteria were met (see "Inclusion criteria"). No limits about the side onset were set for participation in the groups. The opportunity to speak with their speech synthesizer was given to patients with bulbar compromise; all the other participants were invited to respect patients' expression times. Participants chose which daily meeting to take part in at their convenience and two groups were created. Participants who expressed an interest in participating were given an information sheet, and they were contacted by phone to answer any queries, to confirm participation, and to arrange the interview. Informed written consent was obtained from all participants at the time of the interview.

Time and setting
Between December 2018 and July 2019, two psychoeducational groups for people with ALS and their caregivers were conducted at the Respiratory Rehabilitation Unit of the IRCCS Santa Maria Nascente of Fondazione Don Carlo Gnocchi, in Milan (Italy). Each group met for a total of nine monthly sessions of 1 h and a half/2 h each.

Psychoeducation program
A psychoeducation program was developed and delivered by two psychologists at the Unit mentioned above, characterized by speciality trained staff, therapeutic programming, and specific family involvement. The program was facilitated monthly on-site by a psychologist (EV) and a professional of the multidisciplinary team. A program logic model that illustrates the linear flow, the involved professionals, priorities, and topics is shown in Table 1.
The program aims at improving emotional well-being, increasing peer support and awareness, and increasing knowledge and information about the illness and its challenges.

Data collection
Demographic data were collected to describe the sample. Each group session was audio-recorded and transcribed verbatim; then, these transcripts were used to investigate participants' needs. Observations and points of relevant information during and after the sessions filled in field notes. At the end of the program, a semi-structured and iterative interview guide was used to explore perceptions and satisfaction of joint attendance (Table 2). Field notes were completed and prompted questions for future developments. Interviews of approximately 15 min were conducted by a research assistant (VAB) through a phone call. The calls were audiotaped and then transcribed verbatim.

Data analysis
Descriptive statistical analyses were performed using SPSS version 24.0 to summarise the demographic and clinical data and characteristics of the caregivers and patients.
Analysis of transcripts data considered both the group meetings and the semi-structured interviews: the two transcripts have been separately analysed to achieve the two different aims.
Data from sessions were analysed using dimensional analysis and constant comparative method, which are designed to be used with text in grounded theory [35]. These strategies allow the two researchers (EV; VAB) to independently identify both implicit and explicit dimensions of relevant needs and concepts. Data were coded using open, axial, and theoretical coding strategies [40]. The comparative method allowed to detect similarities and differences in the levels of analysis [35].
Analysis of the semi-structured interviews followed interpretative phenomenological analysis (IPA) to better understand patients' and caregivers' experiences and (1) Why did you choose to participate to psychoeducational groups' meetings? Why did you choose to interrupt groups' participation?
(2) Which elements of groups' participation did you find positive? And which elements did you find negative?
(3) Which advice would you suggest improving the psychoeducational groups' experience? (4) Are you satisfied with groups' participation?
perceptions of the program [36]. Each interview was read several times to gain an overall impression of it. Researchers made notes in the margins about the content and the language used by the interviewees. Phrases, keywords, and idiosyncratic features of speech were highlighted. By rereading the interviews, notes have been transformed into themes and sub-themes. Finally, the themes obtained were ordered in a table.
Analysis of audio recordings, process notes, and exit interviews were conducted for triangulation. Discrepancies in theme categorization and coding were addressed by a third researcher (FP) in both the GT and IPA.

Characteristics of the sample
Thirty patients and caregivers were approached and assessed to take part in the study: 9 refused to participate, 3 have been excluded due to cognitive impairment (ECAS < 105), and 18 joined the sessions. The sample included 5 ALS patients and 13 caregivers. The mean age was 67.2 (SD = 11.16) for patients and 61.38 (SD = 14.35) for caregivers. Table 3 shows patients' and caregivers' characteristics. After the end of psychoeducational group sessions, eight participants (2 patients and 6 caregivers) underwent a semi-structured interview.

Themes and sub-themes emerged from transcripts
The main findings that emerged from the psychoeducational program sessions were organized into 7 key themes and 21 sub-themes (Table 4). The key themes represent the need expressed by participants; among them, the need for practical advice and the need for an explanation of the pathology were the most frequent. Table 4 also displays the most frequently used words and the percentage of covered text for each theme.

Theme 1: Practical advice
The first theme that emerged was the need for practical advice, which regarded not only patient's management at home but also interpersonal relationships.

Theme 2: Explanation of pathology
The theme Explanation of pathology referred directly to the psychoeducational nature of the groups since all the professionals explained some important issues in the ALS (i.e., symptoms and progression pathways of ALS).

Theme 3: Recognition of emotions
Participants shared their difficulties in naming, recognizing, and sharing their feelings and emotions. The group itself allowed participants to understand that negative emotions are common among people experiencing the same difficult situation.

Theme 4: Adaptation
The fourth theme that emerged was the need to adapt to this new uncomfortable situation since ALS made it necessary to reorganize patients' and caregivers' lives.

Theme 5: Family and relationships
Participants often spoke about their relationships. After the onset of ALS, their relational world changed, and patients and caregivers often felt alone.

Theme 6: Being caregiver of oneself
The theme being caregiver of oneself only regard caregivers, which often found it difficult to spend time in Table 3 Patients' and caregivers' characteristics

Patient care management at home
Caregivers were concerned about patient care management at home: difficulties with feeding and use of NIV. They frequently discussed about the possible solutions to find out support of home assistants and associations

Interpersonal relationship
Problems in interpersonal relationships concerned how to behave with home assistants, with who it was important to balance between an exclusively work relationship and a family or friendship relationship This made it easier to legitimize this difficulty and negative emotions as normal issues

Loneliness and choice of isolation
For some (n = 4) loneliness was an uncomfortable condition; experienced as something negative and it seemed that there was no one to count on. Others (n = 4) told about loneliness as something chose to protect themselves from the reactions that other people might show; isolation seems to be functional to protect against the feeling of shame

Exit from home
Caregivers often complained about patients who do not want to leave their houses. The group was useful to show how similar this difficulty was present in many patients and to normalize the situation

Sharing life experiences and difficulties
Participants often described life experiences, reporting experiences about the diagnostic process and the difficulties with diagnostic communication, with the adaptation to the disease and with the use of some tools as NIV

Sharing as an opportunity
Participants understood that they were not alone in this situation. In this process, a kay point was the help of professionals who gave information and advice to better cope with the ALS. They made participants feel less alone and more supported self-caring, due to a large amount of time spent taking care of the patient's need.

Theme 7: Sharing
The most important theme is the need to share. One of the most important functions of a group intervention was the possibility to share feelings, emotions, and experiences with others living the same situation.

Connections between themes
Interestingly, connections were found between different themes. Firstly, the themes recognition of emotions and family and relationships were both most present in the third and the seventh group meetings; it also emerges that the emotional theme and the relational theme were both present in meetings 1, 2, 3, 5, 6, 7, and 8; while family and relationships are present alone in session 4. That could suggest a link between the two themes ( Fig. 1). Secondly, caregivers often linked the theme of being a caregiver of oneself to the relational one, because they find it extremely difficult to maintain their relationships after the onset of ALS in their relatives; this connection is shown in Fig. 2.

Themes and sub-themes emerged from semi-structured interviews
Interviews' analysis allowed to understand participants' perceptions and satisfaction about group meetings. The 3 themes and 4 sub-themes that emerged from analyses are shown in Table 5. The identified emerged themes regarding the reasons why patients and caregivers took part in the psychoeducation program and the positive/negative aspects of participation. Moreover, participants generally felt satisfied with the group's attendance and expressed appreciation for this activity. Some (n = 6) also expressed the will to carry on group meetings.

Discussion
The present study explored the needs that emerged in psychoeducational groups for patients with ALS and their caregivers as well as their experiences of participation. Analysis of the group sessions and interviews showed that many participants chose to attend the groups to find information about their illness or their caregiver's one, as also highlighted in previous studies [33,41]. Receiving information about ALS and ALS's progression was a crucial point, especially for caregivers, who reported feeling more confident after group participation. Passoni et al. (2014) also highlighted this point, showing that when caregivers were sufficiently informed about their patient's illness, they felt less anxious [41]. There was no previous literature on the reason why participants leave groups for patients with ALS and/or for their caregivers; this was a new element proposed by the present study.
Practical advice was one of the emerging themes and one of the participants' most appreciated elements, as Locock and Brown had previously shown [32]. Locock and Brown (2010) and Passoni (2014) highlighted the   Reason for participating -Seek information about the disease and the disease progression or about patient care (n = 6); -Confront with others who are all in the same situation (n = 3); -Desire for a comfortable place to share emotions and difficulties (n = 2); -Share a route with the patient they care for (n = 2); -Need of a place to be listened to without being judged (n = 2)

Reasons for leaving
The reasons why participants have left group's attendance could only be asked in one single case. This person referred that she was forced to interrupt group's attendance because of an extremely negative emotional reaction after the first two group meetings and because of the worries about what other participants could think listening her stories about her husband's disease (this patient was in a severe ALS condition, more severe than the other participants' one) Positive and negative aspects 27% Positive aspects -Opportunity of sharing and of support that the group can provide; -The big amount of information shared in the group; -The group could be a reference point that can help in facing difficulties Negative aspects -The difficulty in participating in a group in which levels of disease progression were different. Most of the conversations, in fact, were about disease progression and listen to this was very difficult for patients at the first stage of ALS. Participants often referred that they were distressed after group meetings -The joint participation of patients and caregivers Which advice to improve? 8% -Participation of other professional figures that could be important in ALS management, such as a nutritionist and an otorhinolaryngologist which could provide important information -Restrict participation only to caregivers in order to inform them about the disease and its progression more in detail importance of sharing experiences and emotions in a group composed of people that live in the same situation. This theme emerged also in the present study both as a frequent topic in the transcripts and as a positive aspect reported in the interviews [32,41]. Practical advice (18% of covered text in session 2 and 19% in session 6), Explanation of pathology (35% of covered text in session 4 and 27% in session 2), and Sharing (14% of cover text in session 3 and 10% in session 6) represented the most common topics that participants spoke about; thus, they probably are the fundamental themes, while the others come consequently. Previous studies did not broadly analyse the familiar and relational theme, which instead was investigated by the present study. Locock and Brown focused on Isolation as a choice made by patients with ALS to protect themselves from negative emotions, like shame. This theme also come up from the analysed group sessions [32]. Moreover, Cipolletta et al. (2018) examined support groups for caregivers and found that caregivers often referred to patient care as a duty. The present study, which highlighted the Duty of care as a sub-theme, is coherent with this previous qualitative research [31]. Adaptation was the last important theme in this study. Previous literature about group interventions for people with ALS and/ or their caregivers had analysed this theme. First, Marconi et al. (2016) showed that meditation training for people with ALS and their caregivers improved their acceptance of the disease and the restrictions due to the symptoms [42]. Later, Cipolletta et al. (2018) referred to the caregivers' acceptance of ALS; however, since their groups were not including patients, they did not mention the adaptation of the patient to illness [31]. Our results suggest potential benefits of the psychoeducational group intervention for people with ALS and their caregivers. Previous research often highlighted the importance of taking care of caregiver; our study focuses on caregiver using a psychoeducational methodology. Participation in psychoeducational group may help to increase the perceived control and the self-efficacy in caregivers by receiving information and coping strategies from the multidisciplinary care team and from other caregivers in the same condition [16,34,43]. Thus,caregivers can feel more less anxious and more confident in taking care of the patient and this could also benefit to the patient himself.
Group participation could also reduce caregivers' denial as it allows them to become more aware of their situation and to accept negative emotions and thoughts [34]. Hsieh et al. (2015) found that psychoeducational programs for caregivers are useful to reduce the level of burden in FTD-ALS spectrum; our results suggest that psychoeducational programs could reduce burden by providing information and coping strategies even when patients do not show FTD's symptoms [44].
Psychoeducational groups can be useful also for patients, which can have an experience of social support, that could improve their quality of life and reduce depression linked to disease progression [45]. Moreover, people with ALS can share their emotions about disease progression and symptoms; that could allow them not to use denial as a defence.
To the best of our knowledge, there are no studies that investigated aspects that patients found negative in participating in group's sessions, nor about advice to improve the group's meetings. Our results suggest that supportive counselling is typically characterised by a psychoeducational nature, even more so in a group context, and is useful in progressively disabling illnesses, such as ALS, which implies an incessant and uncontrolled loss of function. Based on what emerged from our study, it would be preferable to be able to follow patients who have the requisites and the desire to do so in a group context, from the earliest stages of the pathology, in parallel with individual paths that allow them to elaborate their personal experiences which, in a group, might not be able to be adequately deepened or might not find the appropriate setting.

Strengths and limitations
One of the most relevant strengths in this study was the novelty of the topic because there was no previous literature about the psychoeducational group for people with ALS and their caregivers. Compared with the individual psychological treatments, group intervention has some strengths: first, it favours the sharing of information, experiences among people who lived the same situation; second, patients with the different conditions of ALS and their caregivers could learn some tips and useful information to daily deal with the illness. Moreover, in a group composed of people in the same situation, emotions could be expressed, understood, and shared without the fear of judgment.
Another positive element was the nature of the analysed data, which came both from transcripts of group meetings' sessions and interviews. Regarding the interviews, their novelty was represented by questions about reasons why either patients or caregivers decided to participate or to leave the group.
The psychological group intervention has also some limits: people at different degrees of ALS can see the condition of the other and they could feel scared about illness progression and its physical and psychological implications. Moreover, it is important to consider that not all patients and caregivers are comfortable in the group, some may feel judged and limited in the expression of their emotions and problems.
The main limitation of this study was the limited number of participants and the restricted geographic area of the sample. A limited number of participants is a common key problem in ALS similar research [31,33]. The approach may be limited to a self-selected sample and limited the generalizability of the results. Only frontotemporal dementia was considered as an exclusion criterion for participation; the other cognitive alterations were not assessed and that was a limit. It would have been appropriate to administer a more complete neuropsychological battery to assess other cognitive impairments.
A further limitation of the study is that it did not consider the effect of parallel psychopharmacological treatment (e.g., antidepressants or anxiolytics) on the psychoeducational intervention.
Moreover, it was not possible to interview all the participants, so we do not have feedback from all patients and caregivers. Given these constraints, additional data comparison would have provided more robust results.

Future implications
There is a need for further studies to better understand the experience of participation in groups for people with ALS and their caregivers. Future studies ought to be conducted with a larger sample and in different geographic areas, or else by using a quantitative research method. Such a strategy could offer the possibility to make comparisons between different times about important issues as anxiety, quality of life, and caregivers' burden. It might be even useful to administer a semi-structured interview before the beginning of the group's meetings to better understand participants' expectations. Lastly, future research should compare the different themes that could emerge in other types of groups for the patient with ALS and/or their caregiver.

Clinical and research implications
The intervention based on psychoeducational groups represents a possible help for patients and caregivers facing ALS. The perceived benefits support the use of the program as an intervention and identified challenges can be used to build a tailor-made program to improve inclusivity and manage group dynamics. Indeed, an intervention that keeps together the element of support and the element of multidisciplinary could be very useful in addressing the complex needs of ALS patients and their caregivers.
On the other hand, our knowledge about psychoeducational groups for people with ALS and their caregivers need to be expanded. This study showed the difficulties found in carrying on research that involves participants who fight against a neurodegenerative illness [46]. As highlighted by the EFNS guidelines on the clinical management of amyotrophic lateral sclerosis (MALS), future research on the psychosocial determinant of quality of life in patients and their caregivers is needed. Future studies are essential to verify the efficacy of this psychoeducational intervention to introduce this practice in the next guidelines for ALS management [47]. The EFNS guidelines on the clinical management of amyotrophic lateral sclerosis (MALS) recommend considering the needs of caregivers and providing them psychological support [47] and, in our opinion, this could be reached using a psychoeducational methodology.

Conclusion
This study of psychoeducational groups for patients with ALS and their caregivers indicates the utility of this type of intervention in supporting people who fight against ALS because of two main reasons: first for the element of psychoeducation provided by professionals; second for the possibility of sharing experiences and emotions with people in the same situation.