Non-alcoholic fatty liver disease (NAFLD) is the most prevalent liver condition worldwide, affecting an estimated 25 % of the population(Reference Younossi, Koenig and Abdelatif1). NAFLD is closely linked to metabolic dysfunction(Reference Abenavoli, Milic and Di Renzo2) and highly prevalent in people with type 2 diabetes and CVD, with the co-morbid presence of steatosis independently associated with adverse cardiovascular events(Reference Meyersohn, Mayrhofer and Corey3,Reference Anstee, Targher and Day4) .
In the absence of proven pharmacotherapy, primary therapy for NAFLD remains focused on lifestyle factors. Weight loss targets of 7–10 % body weight are generally accepted to reduce hepatic steatosis and liver injury(5,Reference Chalasani, Younossi and Lavine6) . However, in the absence of weight loss, an acknowledgement of the value of diet quality is emerging in some practice guidelines(5,Reference Plauth, Bernal and Dasarathy7,Reference Eslam, Sarin and Wong8) . The Mediterranean dietary pattern (MDP) promotes regular vegetables, fruit, extra virgin olive oil, legumes, nuts, herbs and spices, fish and seafood; moderate white meat, eggs and dairy foods; and limited red meat and processed food consumption(Reference Davis, Bryan and Hodgson9,Reference Willett, Sacks and Trichopoulou10) . The MDP is superior to a low-fat diet for long-term weight reduction(Reference Nordmann, Suter-Zimmermann and Bucher11) and has been shown to reduce hepatic fat in the absence of weight loss(Reference Ryan, Itsiopoulos and Thodis12). Strong evidence shows that the MDP reduces risk of type 2 diabetes and CHD(Reference Dinu, Pagliai and Casini13,Reference Estruch, Ros and Salas-Salvadó14) . Proposed mechanisms for a beneficial effect of the MDP in NAFLD include decreased lipogenesis, insulin resistance, oxidative stress, inflammation and fibrogenesis(Reference Zelber-Sagi, Salomone and Mlynarsky15,Reference Berná and Romero-Gomez16) .
It is unknown whether the MDP is recommended by clinician’s managing patients with NAFLD. For translation of evidence into practice, it is important to consider the feasibility of implementing the MDP in routine care, particularly in multi-ethnic settings. An intervention trial in Northern Europe reported barriers and facilitators to MDP adoption for patients with NAFLD through qualitative interviews(Reference Haigh, Bremner and Houghton17), but no qualitative study has reported the perspectives of health practitioners. A recent survey of clinical dietitians in Australia demonstrated an evidence–practice gap in use of the MDP for management of chronic diseases in standard care, including NAFLD for which the MDP was recommended routinely by less than one-third of participants(Reference Mayr, Kostjasyn and Campbell18). Both patients with NAFLD and treating clinicians have highlighted the need for a multidisciplinary team to support lifestyle management of this condition(Reference Avery, Exley and McPherson19).
Therefore, the aim of this qualitative study was to explore multidisciplinary clinicians’ perspectives on whether the MDP is recommended in routine care for patients with NAFLD and the barriers and facilitators to its implementation through semi-structured interviews.
Methods
This qualitative study was designed and reported in accordance with the consolidated criteria for reporting qualitative research (COREQ) checklist (online Supplementary Table S1)(Reference Tong, Sainsbury and Craig20). The study was conducted in line with the Declaration of Helsinki, and the protocol was approved by Metro South Human Research Ethics Committee (HREC/2019/QMS/52598). Informed consent was obtained from all participants.
Participants
Potential participants were initially identified purposively by the research team followed by recruited clinicians initiating snowball sampling. Invitation to participate was via email from the lead investigator (H. L. M.). Eligible participants were clinicians (allied health, medical or nursing disciplines) who were routinely managing patients with NAFLD within the metropolitan public service Metro South Health, Queensland, Australia, who were identified as having a role related to dietary care or referrals for this. One site ran a 12-week NAFLD integrated care clinic (ICC) incorporating medical (hepatology and specialist general practice) and lifestyle (dietetics, exercise and psychology) approaches. Sample size was determined by the number of eligible clinicians who agreed to participate. We acknowledge that an international consensus panel recently suggested metabolic-associated fatty liver disease as the most appropriate umbrella term to define fatty liver disease associated with metabolic co-morbidities(Reference Eslam, Newsome and Anstee21,Reference Valenti and Pelusi22) . At the time this study was conducted (November 2019 to February 2020), metabolic-associated fatty liver disease nomenclature had not been proposed; hence, we have used NAFLD to accurately represent participants’ perspectives.
Data collection
Semi-structured individual interviews were conducted face-to-face or via telephone by the lead investigator (H. L. M.) in the participants’ workplace. Only the interviewer and participant were present during the interviews. Because the interviewer worked as a researcher at one of the recruitment sites, professional interactions had occurred with approximately half the participants prior to the interviews. Interview schedules, which included key questions and potential prompts, differed between dietitians and other clinical disciplines (online Supplementary Tables S2 and S3). These were piloted with a dietitian and gastroenterology consultant and amended to improve readability. Interviews were audio-recorded, transcribed verbatim using an online audio to text automatic transcription service (Temi, 2020) and checked for accuracy by H. L. M. prior to analysis.
Data analysis
Descriptive analysis, performed using Microsoft Excel (2016, Microsoft Corp.), was utilised to summarise participant characteristics with data presented as counts or mean and standard deviation and total range. Transcripts from each interview were transferred to and managed using Microsoft Excel (2016, Microsoft Corp.) and coded and analysed for themes using thematic content analysis(Reference Braun and Clarke23). A deductive style was employed with key research questions and the Theoretical Domains Framework (TDF) informing coding. The TDF is a theoretical framework designed to identify influences on health professional behaviour related to implementation of evidence-based recommendations and has fourteen domains: knowledge; skills; social/professional role and identity; beliefs about capabilities; optimism; beliefs about consequences; reinforcement; goals; memory, attention and decision processes; environmental context and resources; social influences; emotion; and behavioural regulation (see online Supplementary Table S4 for further explanation)(Reference Cane, O’Connor and Michie24). A second investigator (J. T. K.) read a sample of transcripts for familiarisation and to inform the coding framework. The lead investigator coded all transcripts independently. Coded transcripts were reviewed by the second investigator and edited to incorporate feedback and then reviewed by a third investigator (I. J. H.) for triangulation. Dietitian transcripts were coded, reviewed and discussed by the three investigators first, followed by other clinician disciplines. Throughout this process, themes and subthemes, with mapping to TDF domains, barriers and facilitators to practicing MDP and illustrative quotes, were identified and consolidated before final review and discussion involving a fourth investigator (G. A. M.).
Results
Participants
Of nineteen eligible clinicians invited to participate, fourteen were recruited and interviewed (Table 1). All participating clinicians worked in secondary care as part of multiple specialist outpatient gastroenterology/hepatology clinics at one of two hospital sites. Five participants worked in the NAFLD ICC. Non-specialist services for chronic disease management within the relevant public health service were eligible; however, none of the nurses, dietitians or allied health professionals invited from those services identified as routinely treating patients with NAFLD, and in some instances, this was due to NAFLD not being considered eligible referral criteria. Across participants, there was a wide range of time spent in their current clinical role, management of NAFLD patients and working at their respective sites (Table 1). Most clinicians chose to undertake their interview via telephone.
Characteristics of multidisciplinary clinicians participating in individual qualitative interviews
Themes
Four overarching themes with twelve subthemes emerged from analysis of interview transcripts which are summarised, including symbols for inter-related subthemes, in Fig. 1. The link between themes, TDF domains, barriers and facilitators to the implementation of the MDP in routine care, and illustrative quotes is summarised in Table 2. Participants are identified by clinical role only.
Schematic of themes from interviews with non-alcoholic fatty liver disease (NAFLD) clinicians. The central circle presents major themes with facilitators to practicing Mediterranean dietary pattern (MDP) in white and core perceived barrier in black. Outer grey boxes present subthemes; those with matching bullet symbols are inter-related.
Themes associated with Theoretical Domains Framework (TDF), barriers and facilitators to practicing the Mediterranean Dietary Pattern (MDP) and illustrative quotes from data generated by clinicians treating patients with non-alcoholic fatty liver disease (NAFLD) in secondary care
ICC, Integrated Care Clinic.
* Clinical roles: D, dietitian; M, medical doctor; N, nurse. Numbers are random order to distinguish quotes.
Lifestyle modification is primary treatment for non-alcoholic fatty liver disease
Clinicians described lifestyle modification as the most important aspect of management for patients with NAFLD, with a focus on weight loss, diet alteration and increasing physical activity. Most clinicians emphasised that improvement in diet quality was a parallel goal to weight loss and that focus of dietetics education had transitioned away from ‘calorie counting’ to a more food-based diet quality approach which emphasised ‘long-term lifestyle changes’. There was acknowledgement that improvement in diet quality has its own benefits ‘irrespective of weight loss’.
Clinicians of all disciplines identified a role in dietary management. The doctors and nurses, who typically review patients first and/or generate referrals to dietetics, described their role as ‘raising awareness’ of diet’s role in NAFLD development and as the ‘cornerstone of management’. Many also indicated that they do a ‘brief’ diet assessment and education and felt this was expected by most patients. The dietitian role was viewed by most as conducting a detailed diet assessment and counselling with individualisation. Dietitians expressed the importance of having the doctors reinforce diet’s role to enhance patient’s motivation for behaviour change. Challenges that doctors acknowledged were their lack of training and skills in dietary assessment and counselling and that some patients were ‘unwilling to have appointments’ with a dietitian.
The MDP was viewed as an evidence-based dietary approach for both improving diet quality and achieving weight loss and was recognised as reducing risk of chronic co-morbidities such as CVD and type 2 diabetes. Some clinicians, particularly dietitians, referred to evidence for improvement in disease risk factors such as hepatic steatosis, insulin resistance and inflammation with the MDP. Some doctors raised that the evidence for NAFLD is not strong but ‘emerging’ and it is difficult to determine the effects of dietary changes independent of weight loss; nonetheless, the consensus was that the MDP was currently the most evidence-based diet choice. Some doctors and nurses had limited knowledge of specific literature to support clinical benefit of following MDP; however, they were aware of its inclusion at professional meetings and/or clinical guidelines and described it as ‘very topical’ or ‘popular at the moment’. Therefore, both knowledge of the scientific rationale and environmental context impacted on belief in diet recommendations. It was also raised that clinical trials of the MDP may not reflect ‘real life’ and that their patients with NAFLD might not experience the same health benefits as those observed in clinical trials.
Recommending Mediterranean dietary pattern is part of routine care
All dietitians and most doctors and nurses indicated that the MDP was the core dietary recommendation they give to patients with NAFLD. They frequently referenced a ‘Mediterranean-style’ approach which informed education around foods and macronutrient distributions. A minority of participants raised that a potential competing dietary priority to recommending MDP was the ‘high protein, low salt focus’ in patients with cirrhosis.
Having an in-depth knowledge of the MDP supported its implementation in practice. Dietitians demonstrated a comprehensive understanding of core foods promoted versus discouraged, including cuisine elements, and had self-confidence to counsel on the broader pattern followed by patient-centred strategies. Dietitians acknowledged that they had accessed recent literature or professional development describing the MDP in detail and how to implement it, which was necessary for practice integration. Other clinicians mostly understood core food-based principles, for example, extra virgin olive oil; fruit and vegetables; legumes; fish; whole grains; with reduction in red meat and processed foods. Where accessed, knowledge of the MDP was drawn from a Mediterranean diet pyramid, which clinicians acknowledged also emphasises ‘social elements of eating including sitting down for meals’. Wine was recognised as a dietary inclusion but was intentionally not promoted. The minority of clinicians who did not routinely recommend MDP to patients seemed to have a limited understanding of what the MDP encompasses, especially of core foods (e.g. illustrative quote from doctor M2 in Table 2), and they talked about it as a prescriptive ‘diet’.
A key facilitator for inclusion of the MDP in routine care was access to patient education tools and resources. It seems that the recent implementation of an ICC model of service delivery for NAFLD had driven the development of a dietary handout focused on MDP, including a Mediterranean diet pyramid(25), that is shared with all clinicians across the hepatology clinics at that site. This handout provided a simple ‘visual cue’ to guide patient education and acted as a reminder for doctors and nurses to incorporate MDP in their management plan. Some clinicians used one of two short MDP adherence scores(Reference Schröder, Fitó and Estruch26,Reference Álvarez-Álvarez, Martínez-González and Sánchez-Tainta27) which guided patient goal setting and were a tool for monitoring diet quality changes alongside weight. Nurses and doctors unaware or without access to MDP education resources or monitoring tools recommended this diet less routinely and suggested that a specific resource would facilitate practice if available.
Dietary practices are driven by service culture
The dietary practices of clinicians, including dietary education priorities and professional roles, were also driven by the culture of the health services they worked in. Establishment of the ICC with an interdisciplinary team of medical and allied health professionals had facilitated development of clinic guidelines and aforementioned education resources. A focus on improving diet quality through MDP alongside weight loss appears to have become the directive at that clinic, described by clinicians as their ‘mantra’ or that it had been ‘enforced’.
Knowledge sharing between clinicians, with the expertise of dietitians highly valued, was an additional facilitator to practicing MDP in the context of both improved understanding of the dietary pattern and supporting evidence. This was facilitated when dietitians were ‘co-located’ in specialist clinics. The dietitians acknowledged that their own MDP knowledge and skills had been supported by experts conducting research in their local dietetics department. Doctors and nurses who did not have access to a ‘departmental guideline’ or who were less exposed to dietitians were unsure what the focus of their colleagues dietary advice was, had less understanding of the MDP and did not recommend it routinely. These clinicians suggested that ‘in-service’ from dietitians would be an important mechanism to enhance their use of MDP.
Concerns were raised that dietary advice may differ in community settings where health professionals in primary care providing education may not have specialised training in NAFLD. Many expressed that it was more appropriate for long-term patient management to be delivered in a community health setting rather than hospital clinics, but there was currently no mechanism for communication between the two levels of care and hence no feedback on patients after discharge from the hospital clinics.
Perceived challenges for patients to implement Mediterranean dietary pattern
Perceived barriers were predominantly patient-focused. Patients’ culturally diverse backgrounds and long-held unhealthy eating patterns, with a heavy reliance on convenience foods, were key perceived challenges to aligning diet education with MDP. In some instances, there was a lack of belief about the patient’s capabilities to change behaviour and that more emphasis should be placed on their ‘stage of change’. Facilitators to support patients included goal setting around changing their diet pattern, counselling on palatability of MDP and how to integrate within other cultural cuisines.
Other perceived barriers for patients were poor health literacy and low socio-economic background. Clinicians described that many patients have a knowledge deficit of diet–disease interaction, a lack of social support and limited skills in healthy food purchasing and preparation and that MDP is perceived to be costly. Suggested strategies to overcome these challenges were viewed by all clinicians to be the role of the dietitian. These included providing simple, practical and pictorial education resources, of which experiential learning such as cooking classes would be ideal, centring counselling on affordability and emphasising social support.
Limited clinician time and resourcing also appear to compound the issue of overcoming potential barriers for patient behaviour change. In the hospital outpatient setting, there was limited access to dietitians and/or a lack of long-term follow-up, with patients being discharged to primary care where, as previously described, continuation of care is largely unknown. The involvement of a psychologist and exercise specialist was viewed as ideal to achieving lifestyle changes, but funding was typically not available for these roles and only existed as part of the ICC (for a portion, not all patients) in this instance. The doctors and nurses described having ‘increasingly busy’ clinic demands with short consultation times; hence, the time in which they can discuss diet is very brief and not always a priority. Access to the MDP handout, which patients can ‘read at home in their own time’, enabled doctors to include dietary information in a short consult.
Discussion
Given the evidence for a MDP in NAFLD and its inclusion in practice guidelines, it is important to explore feasibility of translating MDP for NAFLD into routine care, particularly in multi-ethnic settings. Through qualitative interviews, we found secondary care clinicians in an Australian metropolitan health service frequently recommended the MDP. Clinician behaviours were influenced by inter-related psychological, social, professional and environmental factors which were highlighted across four primary themes with twelve inter-related subthemes.
Clinicians described lifestyle modification as the primary treatment for NAFLD patients, with both weight loss and improving diet quality through MDP as priorities for most clinicians. Clinical practice guidelines for NAFLD consistently recommend targets for energy deficit to facilitate weight loss(5–Reference Plauth, Bernal and Dasarathy7); however, there is inconsistency with regard to inclusion of macronutrient or food-based recommendations. European(5,Reference Plauth, Bernal and Dasarathy7) and more recently (published after data collection for this study) Asian Pacific(Reference Eslam, Sarin and Wong8) guidelines recommend MDP and the growing body of evidence that MDP improves metabolic health and CVD risk supports its use in NAFLD(Reference Zelber-Sagi, Salomone and Mlynarsky15,Reference Papadaki, Nolen-Doerr and Mantzoros28) . Long-term maintenance of weight loss after energy-restriction diets is poor(Reference Lemstra, Bird and Nwankwo29), and clinicians in our study acknowledged the MDP may offer a more sustainable approach. Overall, beliefs about consequences (i.e. that MDP improves outcomes) facilitated practicing MDP. These beliefs were influenced by a range of sources such as knowledge of specific scientific evidence or a general awareness of its promotion in a guideline or at professional meetings. Interviews with clinicians in the UK demonstrated that beliefs about consequences (or a lack of) were the most prominent influence on whether guidelines for management of NAFLD were implemented; however, in that study, diet was considered only in the context of weight loss(Reference Hallsworth, Dombrowski and McPherson30).
Clinicians who had more in-depth knowledge of the MDP demonstrated greater self-confidence to educate patients. Dietitians acknowledged the influence of expert mentors to guide their practice. Similarly, European dietitians reported that information from colleagues and experts in the field was prioritised in evidence-based practice, especially in unfamiliar clinical situations(Reference Soguel, Vaucher and Bengough31). Dietitians in Australia, especially those in junior positions, have also expressed a lack of confidence in applying knowledge translation to their practice, and greater workforce development is required(Reference Young, Olenski and Wilkinson32). In the context of the MDP specifically, dietitians in Australia have also indicated that direction to up-to-date scientific literature and access to evidence summaries, as well as professional development focused on what the MDP is and how to implement this with patients, would support integration in practice with chronic disease patients(Reference Mayr, Kostjasyn and Campbell18). Some doctors described a lack of dietetics training as a major barrier to assessing and counselling patients on diet and that professional development from dietitians can overcome this. Literature supports that limited nutrition education provided to medical students affects their knowledge, skills and confidence to provide nutrition care(Reference Crowley, Ball and Hiddink33).
Patient education resources based on MDP assisted education and goal setting, while sharing these with multidisciplinary colleagues facilitated MDP recommendations. Developing educational tools for patients and other clinicians has been shown to facilitate dietitians actively seeking and reading the scientific literature(Reference Soguel, Vaucher and Bengough31), and dietitians have indicated that greater access to practical education resources for patients would facilitate MDP implementation in their practice(Reference Mayr, Kostjasyn and Campbell18). Dietitians in the current study described that involvement in developing education resources had supported their MDP knowledge and skills. For doctors and nurses, access to a hardcopy handout supported their memory and clinical decision processes, allowing them to incorporate MDP into short appointments, while the content (particularly a visual MDP pyramid(25)) was a source of education. Patients with NAFLD have described that tools and resources are needed to support ongoing management, while clinicians recognise that monitoring tools are important for behavioural regulation(Reference Hallsworth, Dombrowski and McPherson30). For the clinicians interviewed in our study, use of a MDP score helped but difficulties remained in regard to sufficient follow up to monitor change. Innovations in digital tools may improve patient access to dietary information and monitoring long-term(Reference Morton, Dennison and May34).
The organisational culture and professional roles were identified as important influences on implementation of dietary evidence into practice. The ICC had established an interdisciplinary team (i.e. disciplines collaborate, share knowledge and practice across professional roles(Reference Choi and Pak35)), including allied health, that had developed local guidelines and resources mentioned above. Clinicians who were not linked to the ICC, even some from the same site, had poorer knowledge of MDP and were not aware what dietary advice was being given by their colleagues. Whether practicing MDP or not, diet was viewed as part of each profession’s role with consistency of advice valued. Contradictory dietary information remains prevalent in chronic disease management and is a recognised barrier to changing behaviour(Reference Meyer, Coveney and Ward36). Training all professions within the clinical team on diet for NAFLD, including as a pillar of management and core evidence-based dietary principles, is needed to facilitate a consistent approach(Reference Hallsworth, Dombrowski and McPherson30), and our study found that expert dietitians can provide this training. Concerns that dietary education may differ in primary care, where NAFLD is underappreciated(Reference Patel, Banh and Horsfall37), also highlight that upskilling and communication with non-specialist clinicians would improve continuity of care.
A core barrier to implementation of the MDP was a lack of belief in capabilities of people with NAFLD to change dietary habits, which was inter-related to alleged limited resourcing of clinicians to support patients to do so. Contrary to these beliefs, a recent feasibility trial in NAFLD patients in Northern Europe found one dietitian session using personalised behavioural strategies and practical resources on ad libitum MDP improved diet adherence, reduced weight and increased HDL-cholesterol after 12 weeks(Reference Haigh, Bremner and Houghton17). Patients perceived high acceptability of MDP, which was supported by enhanced nutrition skills. Cost was not an obstacle, and sociodemographic characteristics were not associated with intervention adherence, whereas poor understanding about NAFLD and dietary risks affected intrinsic motivation to follow MDP advice(Reference Haigh, Bremner and Houghton17). NAFLD patient’s perspectives highlight that clinicians may place unnecessary emphasis on potential social barriers. Non-dietetics clinical roles could enhance diet change by prioritising education on diet–disease relationship and consistently reinforce dietitians’ education on MDP. Dietitians should use behaviour change strategies that empower patients and improve self-efficacy(Reference Zelber-Sagi, Bord and Dror-Lavi38). Within limited healthcare resources, integration of virtual care, online tools and group sessions are strategies that could support longer-term care whilst maintaining personalised interactions(Reference Haigh, Bremner and Houghton17,Reference Morton, Dennison and May34,Reference Dobrusin, Hawa and Gladshteyn39) .
To our knowledge, this is the first qualitative study reporting clinicians’ perspectives on recommending the MDP in routine care and our analysis is novel in its comparison of professional roles. The identified barriers and facilitators with mapped TDF domains can be utilised to support intervention strategies for broader uptake of the MDP in real-world practice in other multi-ethnic settings. The findings are limited to the perspectives of clinicians (predominantly female) from two metropolitan hospital services in Australia who are typically triaged patients with complex disease. The purpose of this study was to explore practices and perspectives in a local health service context; hence, the sample size was limited to eligible clinicians who agreed to participate, and data may not be representative of all relevant clinicians across other health services. All but one participating clinician was female; hence, the findings may be subject to sex bias; nonetheless, four out of the five eligible clinicians who declined to participate were also female. The interviewer was a research dietitian with expertise in the MDP, which was known by some participants and could have influenced participant’s responses.
Conclusion
Integration of the MDP in routine management of people with NAFLD in secondary care was facilitated by a focus on diet quality, belief in evidence and an interdisciplinary team approach with expert knowledge sharing and access to education resources. Perceived implementation challenges for patients may unnecessarily restrict clinicians from counselling on MDP or referring to dietetics. Training clinicians to educate patients with NAFLD on the role of diet in their condition and focusing MDP education on behaviour change strategies may improve patient motivation, uptake and therefore clinical benefit. Pragmatic trials should explore innovations in delivery of MDP counselling and format of education resources and monitoring tools through virtual means and group settings.
Acknowledgements
The authors thank A/Prof Katrina Campbell, Dr Michelle Palmer and Dr Shelley Keating for their methodological support.
H. L. M. and this study were supported by a Metro South Health’s Study, Education and Research Trust Account (SERTA) Early Career Research Grant. J. T. K. is supported through a Griffith University Postdoctoral Research Fellowship.
Authors have no relevant conflicts of interest to disclose related to the current study. H. L. M. is an investigator on a clinical trial independent to the current study which received financial support from Cobram Estate Pty. Ltd.
H. L. M. conceptualised, acquired funding, designed the study, recruited participants and collected data with support from I. J. H. and G. A. M. H. L. M. led and all authors contributed to analysis and visualisation of the data. H. L. M. wrote the original draft manuscript, and all authors reviewed and edited subsequent drafts of the manuscript.
Supplementary material
For supplementary material referred to in this article, please visit https://doi.org/10.1017/S0007114521001100
