Frailty is broadly understood to be a multidimensional syndrome characterized by decreases in reserve and diminished resistance to stressors , and is present in between 20 and 50% of people living with chronic respiratory disease [2,3,4▪]. The mechanisms underlying the link between respiratory disease and frailty are likely multifactorial, for example, because of sedentary behaviour, mobility impairments, sarcopenia and malnutrition, in addition to having shared risk factors with frailty (e.g. age, socioeconomic status, chronic inflammation, immune dysfunction) [4▪].
In this review, we consider recent advances in our understanding of frailty, how it might be recognized, and its associated impact on people with chronic respiratory disease. We then discuss advances in supportive and palliative care for those with respiratory disease and frailty, including rehabilitation, advance care planning, and integrated care approaches. To identify literature, we searched Medline for articles published between 1 September 2018 and 3 March 2020. We combined relevant MeSH terms and free text synonyms using the following structure: chronic respiratory disease AND (frailty OR palliative care). Searches were restricted to articles published in English.
UNDERSTANDING AND RECOGNIZING FRAILTY IN CHRONIC RESPIRATORY DISEASE
Since our earlier review , the interconnectedness of chronic obstructive pulmonary disease (COPD) and frailty , and the crosstalk between frailty, comorbidity and other age-related syndromes are better understood and articulated . A distinction between age-related and disease-related frailty has been suggested , though in the context of respiratory illness, frailty is likely to be a combination of both. Marengoni et al.[4▪] published a meta-analysis showing a pooled prevalence using the Fried frailty phenotype, which constitutes five criteria: unintentional weight loss, self-reported exhaustion, weakness, slow gait speed, and low-energy expenditure. In people with COPD, pooled prevalence estimates were 56% for prefrailty (people meeting one or two of the criteria) and 19% for frailty (people meeting three or more of the criteria). COPD led to a two-fold increased odds of frailty, and the few included longitudinal studies suggested a bidirectional association.
Guan and Niu [9▪] provide an excellent summary of frailty assessment tools and areas of practice where frailty may add value, including for screening, stratification or to prompt intervention. Their review shows, through empirical studies, how different tools fit different situations. For example, they unpick the Fried frailty phenotype and show utility across outpatient and community rehabilitation services. Through a stakeholder consensus event, outcomes for a combined exercise rehabilitation programme for people with COPD and heart failure were proposed . Profiling of frailty was ranked as at least moderately important for clinical purposes, and as one of the most important outcomes for research purposes. In this context, assessment of physical frailty was deemed appropriate. The Timed Up and Go Test, 4 meter gait speed and Short Physical Performance Battery (SPPB) were flagged as candidate measures, though ceiling and floor effects were acknowledged .
Frailty screening and assessment in the acute setting is also gaining traction. In the review period, Ospina et al. incorporated frailty screening in a proposed evidence-based discharge bundle for people with acute exacerbations of COPD. Most experts recommended a frailty and comorbidity screen during their nominal group meeting, though suggestions on which tool(s) to use were lacking. Chin et al. reported on the feasibility of implementing the Clinical Frailty Scale among hospitalized people with COPD. Frailty assessments were completed on 46/50 people hospitalized over a 10-month period. Increasing severity of frailty was associated with trends in increased cost, length of stay, and discharge to another facility. Interestingly, in a blinded rating compared with nurses, physicians classified people as frailer in about half of cases. This highlights a need to ensure education and training to better standardize routine frailty assessments.
IMPACT OF LIVING WITH FRAILTY AND CHRONIC RESPIRATORY DISEASE
Frailty, disease and disability are known to coexist, with causal interrelationships between each . There is evidence of this in COPD, where frailty is associated with comorbidities , disability  and geriatric conditions, such as malnutrition . There is emerging evidence that these associations are also observed in idiopathic pulmonary fibrosis (IPF) . In people with COPD or IPF, frailty increases with age [14,17]. Alongside this, within COPD, a cross-sectional study found disease severity and exacerbations are also associated with frailty , and a prospective observational study found dyspnoea was associated with worsening frailty over a 2-year period .
Frailty in chronic respiratory disease is associated with poor outcomes, including increased healthcare utilization and mortality. Among people with COPD and IPF, frailty was associated with higher rate of hospitalization [18–20] and longer hospital stay [18,20]. In people with COPD, frailty was also significantly associated with unfavourable discharge disposition and 30-day readmission . There is consistent evidence that increased severity of frailty in respiratory disease is associated with higher likelihood of mortality [18–20,22,23].
There is also evidence that frailty is associated with higher symptom burden, which may contribute to increased use of nonelective care. A pilot study of 50 people with IPF found that frailty was associated with higher fatigue and shortness of breath . A study of 540 people with fibrotic interstitial lung disease (ILD) also found that frailty was associated with worse quality of life, even when adjusting for age, sex, ILD severity and IPF diagnosis . Many of these quantitative outcomes chime with the qualitative experiences captured in a recent study of people with both COPD and frailty attending pulmonary rehabilitation, who described accumulating, multidimensional losses as part of an unpredictable health trajectory (Fig. 1) [24▪]. Together, these findings corroborate previous evidence that people with chronic respiratory disease and frailty experience worse physical and psychological outcomes in comparison to their nonfrail counterparts [25,26].
ADVANCES IN PALLIATIVE AND SUPPORTIVE CARE
Interventions to address frailty and its correlates in chronic respiratory disease are increasingly important. Recent advances, although not always with populations identified as frail, may inform provision of optimal supportive and palliative care for this group. These include exercise and nutritional interventions to directly address frailty , advance care planning interventions to help manage unpredictable health, and addressing multidimensional losses through integrated models of care.
Strengthening reserves through rehabilitation
Two recent literature reviews explore the potential benefits of exercise in strengthening reserves in people with chronic respiratory disease, including those living with frailty. Neder et al. outline how some with advanced COPD and frailty may not show significant physiological improvements from exercise-based interventions (e.g. pulmonary rehabilitation). However, these interventions can still alter the affective component of dyspnoea and improve capacity to tolerate physical activity in this population. Meanwhile, Tanner et al. unpick how the anti-inflammatory effects of exercise may be a mechanism by which many of the positive outcomes of pulmonary rehabilitation are achieved. Given the association of systemic inflammation with ageing and chronic conditions, including COPD, they suggest a role for pulmonary rehabilitation programmes as a generic intervention to reduce risk of frailty.
With these benefits in mind, an abstract from Kennedy et al. in the United States assesses the impact of pulmonary rehabilitation on frailty in 63 people who are potential lung transplant candidates and recipients. Preliminary results showed postrehabilitation reductions in presence of the Fried frailty phenotype, particularly through improvements in gait speed and exhaustion. This builds on previous UK work that not only suggested the potential role of pulmonary rehabilitation in reducing frailty, but also showed frailty was a strong independent risk factor for not completing the intervention . Acknowledging these challenges, Brighton et al.[30▪] conducted a realist review to understand how exercise-based approaches may be better adapted for those with COPD and frailty. Five key principles were identified to help adapt rehabilitation for this group: building trusting relationships, creating a shared understanding of priorities, individualizing content to match priorities, having capacity to address multidimensional losses and having flexibility in service delivery.
Alongside exercise-based approaches, there is growing work to explore nutritional adjuncts. Billingsley et al. conducted a literature review of the role of nutritional strategies to increase cardiorespiratory fitness in a range of conditions, including chronic respiratory disease, and sarcopenia and frailty. There was insufficient evidence to recommend a nutritional adjunct to pulmonary rehabilitation, although these approaches showed promise. Kuniaki et al. also report a case where they explore the potential benefits of the traditional Japanese medicine Ninjin’yoeito to address frailty in a person with COPD. The person's frailty had persisted despite using bronchodilators, nutrition support and pulmonary rehabilitation over 4 months, but showed improvement in both physical and psychological domains 1 month after these measures were supplemented with Ninjin’yoeito taken three times a day. The authors suggest further clinical studies to determine effectiveness.
Managing unpredictability with advance care planning
Adequate care planning will also be important to help manage the unpredictable disruptions to health and subsequent deterioration characteristic of frailty. A scoping review of advance care planning practices within COPD by Meehan et al. identified few trials of advance care planning interventions. The most recent was a multicentre cluster randomized controlled trial (RCT) by Houben et al., testing a nurse-led one and a half-hour home-based advance care planning session in the Netherlands. They recruited 165 people with advanced COPD posthospitalization for an acute exacerbation. Their intervention was associated with increased advance care planning discussions and significantly lower family anxiety at 6 months, in comparison to usual care. This builds on evidence from a previous Australian trial of a hospital-based nurse-led intervention that helped to increase uptake of advance care planning . However, Houben et al. also reported high numbers of people with COPD declining to participate and gatekeeping by professionals, suggesting a need for careful work to implement into routine practice.
New approaches to advance care planning have also been tested in pulmonary rehabilitation and long-term care facilities. Grossman et al.[36▪] evaluated two 1 hour group-based discussions of advance care planning with people attending pulmonary rehabilitation, facilitated by palliative care specialists. Thirty people who attended at least one session found the content relevant and appreciated the opportunity to share their thoughts. Two participants found some of the discussions difficult. Within long-term care facilities, Sussman et al.[37,38] used condition-specific pamphlets to support communication around end-of-life care for people affected by dementia, heart failure, COPD, renal failure, and frailty. Residents and family members reported that the pamphlets supported reflections on future care, but that discussions with each other remained difficult . Although staff who had read the pamphlets (n = 105) felt the information was useful, more staff reported using the pamphlets for self-education than for educating residents and their families. The authors suggested a need for accompanying communication training and a clearer distribution strategy to support implementation.
Perceived challenges from professionals around when and how to implement advance care planning, and feeling inadequately trained to undertake these conversations, are well documented . To guide such training, Burgess Kelleher et al. asked 38 experienced medical, nursing and allied healthcare professionals to identify priority topics for advance care planning education. Areas of strongest consensus included identifying who with COPD might benefit from palliative care interventions and when, identifying changing care needs, addressing mismatches in patient/family expectations, and talking about poor prognosis. Respiratory and palliative medicine specialists across Australia, New Zealand, and the United Kingdom (n = 440) also agree on the need for advance care planning in COPD, suggesting a readiness for greater collaboration and multidisciplinary models of care .
Addressing multidimensional losses through integrated care
Calls for integrated models of respiratory care are well aligned with what is known about the multidimensional losses experienced by those with respiratory disease and frailty [24▪]. As such, approaches that seek to integrate palliative care may be of benefit to this population. For example, a recent systematic review  found that holistic breathlessness services, which typically integrate palliative and respiratory care, are effective in reducing distress and depression symptoms in people with advanced disease and chronic breathlessness. One suggested role of these services was as a bridge to, or step down from, rehabilitation services, for those who are more unwell. However, the authors also acknowledged that triggering these services as part of an earlier palliative care approach might be important. The role for early palliative care in respiratory disease is supported by Iyer et al.'s [42▪▪] recent work with 10 people with COPD and 10 family caregivers: they responded positively to a standardized description of early palliative care, and they felt integration could occur from moderate COPD (GOLD stage II) onwards. This was echoed by 12 clinicians from pulmonary and palliative care , who agreed on the potential added value of palliative care alongside respiratory care.
Several recent trials have now sought to determine acceptable and effective models to deliver early palliative care, but not without challenges. One intervention with promising qualitative feedback was the new outpatient ‘CAPTAIN’ care model in Denmark . This involved community management of those with severe COPD through needs-based (rather than routine quarterly) contacts with the respiratory team, and annual advance care planning dialogues. People who received the CAPTAIN model reported improved quality of care and more continuous and natural advance care planning discussions. Feeling ‘known’ by their CAPTAIN nurse was key to this success. Doctors and nurses delivering the service [45▪] also felt care was more person-centred and holistic. However, increased continuity of care came with increased exposure to suffering, making professionals’ roles more stressful and mentally exhausting. Multidisciplinary support and ongoing supervision were suggested as important in ameliorating this.
Other new trials of home-based approaches also show potential for success. Vitacca et al. conducted a before--after feasibility study of a home-based tele-assisted palliative care intervention with 10 people with severe COPD in Italy. Each received a 60-min advance care planning discussion in hospital, followed by postdischarge monthly telephone support from a nurse specialist. Their intervention was deemed feasible and participants expressed their satisfaction, yet in many cases the person's preferences were not fulfilled when an acute event later arose. In another pilot RCT of early home-based palliative care for people with COPD [47▪▪], people in the intervention group (n = 26) received monthly support from a community palliative care team, whereas those in the control group (n = 23) received usual care. Again, the intervention and data collection were deemed feasible; however, significant problems with recruitment meant the planned sample size (n = 80 per group) could not be reached. Finally, Scheerens et al.[48▪▪] conducted a pilot RCT of a home-based approach for people with COPD in Belgium. People in the intervention group (n = 20, usual care control group n = 19) received on average 3.4 visits from palliative home care nurses over 6 months. The nurses provided protocolized symptom management and support, care plans, and leaflets on coping mechanisms. Their intervention was also deemed largely feasible and acceptable but did not show anticipated effects on participant health outcomes. The study was likely underpowered but the team also suggested a need for increased training of the palliative nurses in COPD management, and greater integration across teams.
Challenges around delivering holistic care and integrated working across relevant professional groups have been commonly noted. This raises the question as to whether models of care that support integration beyond respiratory and palliative care may have most potential, particularly in addressing the multidimensional losses seen in those with frailty. For example, Van Dam van Isselt et al.[49▪▪] report a cohort study of their geriatric rehabilitation service for people with COPD in the Netherlands. The service constitutes a 6-week inpatient multidisciplinary rehabilitation programme, beginning with a Comprehensive Geriatric Assessment and incorporating expertise from respiratory, geriatric and palliative care. Their intervention group (n = 78) showed a significant and clinically meaningful improvement on disease-specific health-status, and experienced significantly fewer exacerbations than the control group who declined the service (n = 80), at 3-month follow-up. Although some caution in interpretation is needed because of natural differences in the groups and risk of confounding, some of these differences were addressed through use of propensity scores. Barratt et al.[50▪▪] also report a retrospective cohort study in the UK, where people with ILD and palliative care needs are reviewed by a multidisciplinary team (MDT). This team includes a palliative care consultant and nurse, a psychologist, an ILD consultant, nurse, and pharmacist, and an MDT coordinator who met every 6 weeks. In comparison to those seen prior to creation of the MDT (n = 26), those seen by the MDT (n = 46) showed increased: documentation of cardiopulmonary resuscitation decisions, referrals to fatigue and breathlessness support and specialist palliative care, recommendations for general practitioners to add them to a supportive care register, and referrals to community matrons. This preliminary work shows the promise of multidisciplinary integrated care approaches for those with respiratory disease at risk of poor outcomes, although further controlled studies focusing on those identified as living with frailty are still needed.
People living with respiratory disease and frailty are at risk of poor outcomes, and likely to benefit from recent advances in supportive and palliative care. Heterogenous trial designs and populations have been cited as a particular challenge in this area of research . However, it might be that more explicit theoretical modelling and consideration of intervention mechanisms would help overcome some of these challenges and support transferable learning across different contexts [30▪]. It is also notable that few studies reported involving people with COPD and their informal carers in their priority settings activities, or research and intervention design. Working more collaboratively with service users may be an important part of improving both research and intervention acceptability.
Lack of agreement over appropriate criteria for early palliative care is evidenced from both stakeholder feedback and varying trial entry criteria (e.g. incorporating long-term oxygen use [47▪▪], MRC dyspnoea [48▪▪] and/or the ‘surprise’ question ). Considering the utility of measuring frailty regardless of diagnosis/comorbidities, and the poor and unpredictable health that often accompanies it, using frailty as an indicator to prompt additional integrated supportive and palliative care may be worth exploring. With little work specifically addressing frailty and respiratory disease, this may be an efficient way to respond to calls for proactive integration of geriatrics and palliative care in respiratory disease .
Recent advances in supportive and palliative care, including rehabilitation, advance care planning and early palliative care, may be of benefit to people living with both chronic respiratory disease and frailty. Models showing integration across multiple specialities and professionals (e.g. respiratory, geriatrics, palliative care) may have the most potential to strengthen reserves and meet the multidimensional needs of this group. Future research should develop and test models of care that specifically address frailty in respiratory disease, including exploring the role of frailty in triggering integrated multidisciplinary input.
Financial support and sponsorship
M.M. is funded by, and L.J.B. is supported by, a National Institute for Health Research (NIHR) Career Development Fellowship (CDF-2017-10-009). M.M. is supported by the National Institute for Health Research (NIHR) Applied Research Collaboration South London (NIHR ARC South London) at King's College Hospital NHS Foundation Trust. The views expressed are those of the author(s) and not necessarily those of the NIHR or the Department of Health and Social Care. A.E.B. is supported by The Dunhill Medical Trust and Cicely Saunders International.
Conflicts of interest
Of the 41 papers included in the review period, L.J.B. is an author on three and M.M. is an author on five. The authors declare no other conflicts of interest.
REFERENCES AND RECOMMENDED READING
Papers of particular interest, published within the annual period of review, have been highlighted as:
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