Conceptualization, use, and outcomes associated with compassion in the care of people with multiple sclerosis: a scoping review

Objective Compassion is widely regarded as an important component of high-quality healthcare. However, its conceptualization, use, and associated outcomes in the care of people with multiple sclerosis (PwMS) have not been synthesized. The aim of this review is to scope the peer reviewed academic literature on the conceptualization, use, and outcomes associated with compassion in the care of PwMS. Methods Studies were eligible for inclusion if reporting primary research data from quantitative, qualitative, or mixed-methods studies on the conceptualization, use, and outcomes associated with compassion in the care of PwMS. Relevant studies were identified through searching five electronic databases (CINAHL, Cochrane Library, EMBASE, MEDLINE, and PsycINFO) in January 2022. We followed the guidance outlined in the Joanna Briggs Institute (JBI) manual for evidence synthesis, and also referred to the Preferred Reporting Items for Systematic Reviews and Meta-analyses extension for Scoping Reviews Checklist (PRISMA-ScR). Simple descriptive methods were used to chart quantitative findings, and a descriptive approach with basic content analysis was employed to describe qualitative findings. Results Fifteen studies were included (participant n = 1722): eight quantitative, six mixed-methods, one exclusively qualitative. Synthesized qualitative data revealed that PwMS conceptualize compassion as involving self-kindness, agency, and acceptance. PwMS report using self-compassion in response to unpleasant sensations and experiences. Quantitative findings suggest that compassion may mediate benefit finding, reduced distress, and improved quality of life (QoL) in PwMS, that those with the condition may become more compassionate through time, and that self-compassion specifically can be increased through training in mindfulness. In this context, greater self-compassion in PwMS correlates with less depression and fatigue, better resilience and QoL. Among studies, self-compassion was the most common outcome measure for PwMS. Conclusions A nascent literature exists on the conceptualization, use, and outcomes associated with compassion in the care of PwMS. Further research is required to better understand what compassion means to PwMS and those caring for them. However, self-compassion can be cultivated among PwMS and may be helpful for managing unpleasant somatic symptoms and in benefit finding. Impact on other health outcomes is less clear. The use of compassion by health care providers in the care of PwMS is unstudied.


Introduction
Multiple sclerosis (MS) is a chronic, progressive, neurodegenerative condition typically diagnosed between 20 and 40 years of age [1]. Around the world, incidence and prevalence of MS are increasing [2]. MS is an expensive condition, both for PwMS and for health services [3]. In the early stages, disease-modifying treatments are associated with most cost. As the condition progresses, social care costs dominate. However, around a third of all costs relate to intangible costs, deriving from patient suffering (stress, pain, fatigue), the so-called 'hidden symptoms' [4]. Indeed, people with multiple sclerosis (PwMS) commonly describe the condition as stressful, yet highlight how emotional aspects of care are frequently overlooked by their healthcare providers (HCPs) [5]. Stress is toxic for PwMS, increasing

Inclusion criteria
Studies were eligible for inclusion if reporting primary research data in English, from any year, inclusive of quantitative, qualitative, or mixed-methods findings on the conceptualization, use, and/or outcomes associated with compassion in the care of PwMS. If including other health conditions, data had to be extractable for PwMS specifically.

Screening and selection
We used Endnote and Covidence to store, screen, and sort results. Two reviewers (SP, RS) independently screened titles and abstracts of bibliographic records derived from the search. After removing duplicates, two reviewers conducted title and abstract review. Pilot testing of source selectors was conducted by assessing a random sample of 25 titles/ abstracts, where our research team screened these using our eligibility criteria. We undertook full screening only once our team achieved > 80% agreement. Our agreement was defined by Cohen's Kappa, κ = 0.83.

Data extraction
Included studies were charted by two independent reviewers using the JBI manual data extraction template [37]. First, we performed a pilot extraction, whereby we trialed the extraction template for 2-3 sources to ensure all relevant results were being extracted. The following data were extracted: author(s), publication year, country, study aims, study type, methodology/methods, population/sample size, intervention/ comparator, outcomes, and findings relating to the conceptualization, use, and outcomes associated with compassion in the care of PwMS.

Analysis
Simple descriptive methods were used to chart the quantitative data, and a descriptive approach with conventional content analysis was undertaken to describe qualitative data [38]. An assessment of study quality was deemed overly complex with little added value given the wide ranging nature of study designs; an acceptable approach within scoping review methodology [36].

Results
Our search in January 2022 generated 1145 'hits'. Following de-duplication, there were 919 records. After title and abstract screening, 16 full text studies were deemed eligible, retrieved, and reviewed; however, one was a duplicate study. Thus, 15 articles were included in the final review. Search results are detailed in Fig. 1.

Intervention characteristics and adherence
Five studies were interventional [10,39,47,50,51], all being "Mindfulness-based"-with the aim being to decrease distress and improve psychological well-being.
Each intervention occurred over 8 weeks, with sessions ranging from 1-to 2.5-h duration, and were facilitated by psychologists or physicians. One intervention ran virtually, over Skype [10], one was conducted across different community-based venues [47], and three were held in a medical clinic [39,50,51]. In the parallel pilot mixedmethods study from Europe, all participants completed four (or more) of eight sessions. In the pilot study from Australia, 80% of participants attended four to five of five sessions. In the RCT from Europe, 60% of participants met the criteria for course completion (> 4 sessions). Of the two mixed-methods studies conducted following a mindfulness-based stress reduction (MBSR) intervention, one reported that 17% of participants did not complete the course [51], while the other reported 18% attrition (Table 3) [50].
In qualitative analyses with posteriori conceptualizations, self-compassion was described as involving an awareness of the need to care for oneself and indeed to be an active agent in this sense, [52] whereas adopting self-kindness towards one's psychological state and physical body were characterized by acceptance, and the active distillation of negative self-talk and self-criticism [10,47]

Use of compassion in the care of PwMS
The use of compassion in the care of PwMS was discussed both in terms of relating to oneself (self-compassion) and in relation to others. Self-compassion was often used during mindfulness training to allow PwMS to replace prior tendencies towards self-judgment and criticism. For example, in a mixed-methods study from Europe, PwMS reported that mindfulness training aided them in developing a sense of compassion and self-directed kindness, rather than feelings of "guilt" and patterns of "negative self-talk" that they experienced previously [10]. One participant reported that she could now, "actually do things on my own and be happy with my own company" rather than seeking comfort and assurance from others [10,50]. In a qualitative study from Asia, mindfulness was evoked by PwMS as being a component of self-compassion, in which one could actively replace ruminating on the "negative impacts" of MS with "selfconstruction and turning the bad feeling into good ones" where self-kindness included "not blaming self because of the disease" [52]. In another mixed-methods study from Europe, PwMS reported that mindfulness training allowed them to learn more about themselves and helped them to "accept their experience" living with illness [47]. Notably, PwMS reported initial difficulties channeling a sense of self-compassion during somatically focused mindfulness practices but that this "changed over time" as individuals eventually felt more "accepting" and "self-compassionate" towards themselves. Another mixed-methods study from Scotland, also reported that PwMS found being attentive to bodily sensations increased awareness of MS symptoms, but that eventually "this initial discomfort with coming face-toface with their MS changed over time, into a more accepting and self-compassionate approach" [50]. In one case, a participant recounted how he was able to replace a previously automatic anger response to painful muscle spasms with equanimity instead: A compassionate approach towards one's experience was also used by PwMS in response to impaired mobility, evoking the idea that for PwMS there may at times be a somatic or functional trigger to practice self-compassion. For example, PwMS reported that while mobility difficulties previously led to negative self-talk and self-blame, such moments now served as a reminder to practice self-compassion [10] In quantitative analyses, PwMS were reported to present themselves in a more passive and compassionate manner compared to healthy controls, which the authors suggested may predispose PwMS to practice social compliance to avoid conflict [45].

Outcomes among PwMS
Across several studies, self-compassion among PwMS varied with self-esteem, mental health diagnoses, QoL, and level of disability. In a mixed-methods study from Europe, participants reported gains in compassion towards oneself since being diagnosed with MS, independent of sex, gender, and ethnicity [49]. In a longitudinal survey study from Australia, factor analysis of the BFiMSS revealed that compassion/empathy was linked to finding benefits within the context of an MS diagnosis, where increased age and time since diagnosis were weakly linked to greater compassion/empathy [44]. A cross-sectional study from Bulgaria indicated that although total self-compassion scores among PwMS did not differ compared with healthy controls, scores on self-compassion subscales did differ according to one's level of disability. Specifically, those PwMS with the highest level of disability reported greatest self-kindness and lowest self-judgment, while healthy controls reported greatest selfjudgment and lowest self-kindness [42].
In other cross-sectional studies, self-compassion was also linked with a variety of physical and mental health outcomes in PwMS. A study from Spain found that after 'strict confinement' due to COVID-19, self-compassion among PwMS was significantly and positively correlated to physical role, social function, vitality, and global health, and negatively correlated with global fatigue and cognitive fatigue [46]. A study from Iran found direct, but statistically insignificant correlations between self-esteem and various subscales of self-compassion, such as self-kindness, and self-judgment [40]. A study from Turkey revealed that non-depressed PwMS had higher self-compassion scores and better QoL compared to those with depression [41]. In another study, compassion was positively related to anxiety and inversely related to depression [44]. A study from the USA found that self-compassion was significantly correlated with QoL as well as resilience [43]. In a study from the UK, self-compassion had small mediation effects in lessening distress immediately following an MBI, with moderate sized effects at follow-up [10]. In a study from Australia, total scores on the Self-Compassion Scale increased for PwMS following 1 3 an MBI, while in a study from Scotland, significant, large, and sustained effect sizes were evident for self-compassion immediately following an MBI and 3 months later [39].

Outcomes among caregivers of PwMS
A longitudinal study from Australia found that factors of the BFiMSS had external validity, as caregiver ratings of benefit finding were positively, and significantly correlated with BFiMSS factors, including compassion/empathy, and overall score among PwMS [44]. In addition, results from a cross-sectional study from Spain indicated that caregivers of PwMS had 'high' compassion scores, and that such scores were not significantly correlated to their mental, physical, global health, or fatigue [46].

Outcomes among HCPs of PwMS
Healthcare provider (HCP) compassion for PwMS was not measured directly in any study. However, in a study from Italy, differences in compassion fatigue emerged according to HCP role as well as age. Specifically, neurologists, compared to nurses, had lower compassion satisfaction and an elevated risk of burnout, although both groups reported high levels of compassion fatigue. Younger (< 45 years old) HCPs had lower compassion satisfaction (i.e., derived less fulfillment from vocational role) in caring for PwMS and higher burnout, although both groups had high levels of compassion fatigue [48]. Table 4 provides an overview of the conceptualization, use, and outcomes of compassion in the care of PwMS.

Summary of findings
This scoping review has explored the conceptualization, use, and outcomes associated with compassion in the care of PwMS. Among studies included in this review, compassion was most often conceptualized based on established, a priori definitions, including compassion in relation to oneself and, as is more traditional, towards others. However, posteriori definitions exclusively described self-compassion, conceptualized as involving self-kindness towards one's psychological and physical being, abandonment of self-criticism, acceptance, and a sense of agency. Quantitative findings suggest that greater compassion may mediate benefit finding, reduced distress, and better QoL among PwMS, that those with the condition become more compassionate through time, and that self-compassion specifically can be increased through training in mindfulness. In terms of outcomes, greater self-compassion among PwMS correlates with less depression and fatigue, better resilience and QoL.

Conceptualization of compassion
Considerable debate remains as to the construct of compassion and its conceptualization generally [11,55]. In the context of MS, very little data exists on how PwMS conceptualize compassion from others, or how HCPs use compassion in caring for those with the condition. This latter point is a notable finding, in part because more general evidence syntheses suggest that compassion is most often studied in HCPs and much less so among patients [11], but also because PwMS value when HCPs attune to their emotional needs and take steps to address their distress [5,56]. Indeed, PwMS report how a perceived lack of empathy from HCPs weighs heavily in the 'cost' they consider when deciding whether or not to seek out help through mainstream health services [57]. This is problematic for many reasons. Firstly, the needs of PwMS are complex and are accentuated at times of greatest stress, such as at diagnosis, during a relapse, or as disability progresses [58][59][60][61][62]. Secondly, many of the symptoms of MS are 'hidden' [63] and therefore may go unnoticed by HCPs, perhaps explaining the lack of attention as perceived by PwMS. However, as the empirical definition of compassion depends upon the recognition of suffering in another, it seems crucially important that HCPs know to ask about 'hidden' suffering, even if not apparent on superficial review, besides how to respond [with compassion] when hidden suffering does exist. If such needs are not met in mainstream services, PwMS may end up paying out of pocket for alternative treatments [64,65] where providers may be perceived as having better 'listening skills' and demonstrating 'more care and concern' [66].
The debate as to the conceptualization of compassion generally notwithstanding, it seems important to better understand what compassion means to PwMS and their HCPs. This type of study has been done previously in palliative care, using a Grounded Theory approach, with findings suggesting distinct and overlapping meanings for compassion between patients and HCPs [67,68]. Pursuing such an approach would appear beneficial in informing care optimization for PwMS, given the current mismatch reported between what care PwMS want, versus what they receive [5,56,57,62].

Use of compassion
In terms of how compassion is used in the care of PwMS, findings suggest that self-compassion is an important factor in the adjustment process, where benefit finding plays a part 1 3 in discovering positive perspectives on life because of, or in spite of, having MS. This fits with the general academic literature on benefit finding, where factor analysis has previously confirmed compassion as an important component in this complex, multifactorial process, along with conceptually similar post-traumatic growth models [69]. However, besides training in MBIs, which addresses compassion broadly and, arguably, indirectly [9], from this review of the literature it seems that compassion is not being used explicitly in the care of PwMS, by either HCPs or caregivers.
Compassion should, in theory, be a core part of HCP treatment of PwMS. However, high levels of compassion fatigue and burnout are reported in key specialties caring routinely for PwMS, including Neurology [70], Rehabilitation Medicine [26], and Primary Care [27], a scenario likely to have been accentuated greatly during the COVID-19 pandemic. Known drivers of compassion fatigue and burnout (time constraints, inadequate staffing, excessive workload, care fragmentation, use of technology, lack of resources, organizational culture) [71] have also been identified as common barriers to the delivery of compassionate care [11]. Compassion fatigue and HCP burnout matter because they are associated with reduced productivity, lower quality patient care, and worse health in HCPs, increased risk of medical errors, increased costs, and lower patient satisfaction [71]. Interventions for compassion fatigue and burnout need to be multifaceted to be effective [72], but arguably should include compassion-based interventions [22,29,73,74]. However, how compassion is defined in this context needs to be considered carefully [75,76] as the link between the empirical definition of compassion [14,75] and compassion fatigue, although perhaps intuitive, is scientifically tenuous at best [77].
Only one study in this review addressed the role of compassion among PwMS within the context of the COVID-19 pandemic [46]. Further study in this area may be beneficial, as in the general population, greater perceived compassion from others and towards one's self are associated with less psychological distress and fears of contracting COVID-19 [78]. Virtual interventions to facilitate increased self-compassion among PwMS may represent an effective way of addressing the surge of psychological distress reported by PwMS during the COVID-19 pandemic [79,80]. Online MBIs appear to be acceptable to PwMS [81], are effective at reducing stress [82,83] and improving self-compassion [69], but do not have compassion as the core focus of treatment and compassion-based interventions may be more effective at improving compassion specifically [9].
Nevertheless, mindfulness and compassion in the care of PwMS appear linked, in that MBI training is associated with an increase in levels of self-compassion while course participants also describe a newfound sense of care and concern for an ailing body. Qualitative research findings in this review certainly suggest that MBI training can help PwMS to develop a more compassionate approach toward themselves, and in relation to others, which may be associated with improved interpersonal functioning and social supports, and fits with existing evidence in general that MBI training is an effective way of improving compassion [29], prosociality [84], and interpersonal relationships [54]. However, learning to be compassionate towards oneself and/or others may take time develop and those PwMS who are older and more disabled report being more compassionate in comparison to younger and less disabled counterparts. When viewed as part of a longitudinal adjustment process, this finding may in part be explained by MS being a 'moving target' [85,86]; particularly in the early stages where fluctuations in disease activity, treatment regimens, and distressing symptoms can be pronounced [87,88], and present the greatest challenges socially [89,90].

Outcomes of compassion
In terms of outcomes, the measurement of compassion among PwMS is a relatively nascent area. Quantitative measures most commonly included the Self-Compassion Scale, which is a six-factor scale including dimensions of self-kindness, self-judgment, common humanity, isolation, mindfulness, and over-identification [91]. Although widely validated in the non-MS literature, this measure has not been validated specifically for use among PwMS, which matters because generic well-being outcome measures may fail to capture what matters most to those affected with MS [92]. Furthermore, the lack of empirical validation for PwMS limits interpretation of findings, in that although there may be face validity for the construct of compassion in the context of managing MS, we cannot be sure about the ecological validity and reliability of the measurement scales in this specific population, as this has not been empirically tested.
Lastly, it is important to determine the outcomes of compassion among caregivers of PwMS. Within the literature examining the experiences of caregivers for older adults, and individuals with dementia, compassion is often linked to compassion fatigue [93][94][95][96]. Findings from this review suggest that the experiences of caregivers' of PwMS are not linked to their QoL and well-being [46], but further research is needed to examine specifically the link between compassion and caregiver well-being within the context of caring for a person with MS.

Strengths and limitations
This scoping review provides a comprehensive examination of the evidence for the conceptualization, use, and outcomes associated with compassion in the care of PwMS. In keeping with the general literature on compassion in healthcare 1 3    [11], findings from this current review highlight gaps in the evidence base, such as the paucity of RCTs assessing the effectiveness of compassion as an intervention for improving outcomes for PwMS, or even more generally how compassion is used by HCPs in caring for PwMS. A wide range of validated measures of compassion have been applied to PwMS but have not been validated in this population per se. Lastly, participants across included studies were mainly "white". This raises the question of how compassion in the care of PwMS from diverse ethnic and racial groups is conceptualized, used, and measured, prompting the need for cultural humility and targeted research across more diverse populations. For example, among some cultures compassion may not be viewed positively in a healthcare context [97].

Implications
Preliminary conceptualizations of compassion among PwMS have been identified in this scoping review, but more qualitative research is needed to better conceive of the meaning of compassion in the care of PwMS, particularly from the perspectives of care partners and HCPs. Once a clear conceptualization is made, then use and outcomes may be more closely scrutinized. Lastly, there is a need to test compassion-based interventions within the context of MS, as most of the synthesized literature reports on MBIs, in which compassion is only a component part [9]. HCPs may wish to consider how to acquire skills in compassion for them to use in their clinical practice, besides how to train PwMS in self-compassion, which seems particularly promising. Recent systematic review evidence on the nature of compassion education reported a large variety of 'humanities-based reflective practices' to facilitate learning about compassion in the context of healthcare [22]. Training practices included reflexive writing, visual analysis of images, watching movies and listening to music [22]. Additional studies indicate that role play and mindfulness may facilitate the cultivation of compassion [73,98] Conclusion A nascent literature exists on the conceptualization, use, and outcomes associated with compassion in the care of PwMS. Further research is required to better understand what compassion means to PwMS and those caring for them. However, self-compassion can be cultivated among PwMS and may be helpful for managing unpleasant somatic symptoms and in benefit finding. Impact on other health outcomes is less clear. The use of compassion by health care providers in the care of PwMS is unstudied.
Funding None.

Conflicts of interest
The authors declare that they have no conflict of interest.
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