Article

A Qualitative Study Supporting Optimal Nutrition in

Advanced Liver Disease—Unlocking the Potential
for Improvement
Shaye Ludlow 1,2, Katherine Farragher 3, Kelly Squires 3, Susan Heaney 4, Jessica Orman 1,2, Sarah Pullen 1,2,
John Attia 1,2,5 and Katie Wynne 1,2,5,*

1 John Hunter Hospital, Hunter New England Local Heath District, New Lambton Heights, NSW 2305,
Australia; shaye.ludlow@health.nsw.gov.au (S.L.); jessica.orman@health.nsw.gov.au (J.O.);
sarah.pullen@health.nsw.gov.au (S.P.); john.attia@newcastle.edu.au (J.A.)
2 Hunter Medical Research Institute, Equity in Health and Wellbeing,

New Lambton Heights, NSW 2305, Australia

3 School of Health Sciences, University of Newcastle, Callaghan, NSW 2308, Australia;

katherine.farragher@uon.edu.au (K.F.); kelly.squires@newcastle.edu.au (K.S.)

4 Department of Rural Health, University of Newcastle, Port Macquarie, NSW 2444, Australia;

susan.heaney@newcastle.edu.au
5 School of Medicine and Public Health, The University of Newcastle, Callaghan, NSW 2308, Australia

* Correspondence: katiejane.wynne@health.nsw.gov.au

Abstract: Malnutrition rates in Advanced Liver Disease (ALD) are significantly higher than those in
well-compensated liver disease. In addition to its physiological impact, malnutrition is detrimental
for quality of life and social, emotional, and psychological well-being. Studies within oncology and
renal supportive care have identified the influence of non-physiological factors on malnutrition risk.
Integrating similar factors into malnutrition screening for ALD could improve identification of at-
risk patients to optimize treatment planning. This qualitative study aimed to understand the holistic
factors influencing nutritional status in the ALD population. Semi-structured interviews with 21
Citation: Ludlow, S.; Farragher, K.;
patients, carers, and clinicians explored the experiences of malnutrition in ALD. Thematic analysis
Squires, K.; Heaney, S.; Orman, J.;
revealed five key themes: (i) appropriateness of healthcare delivery; (ii) health- and food-related
Pullen, S.; Attia, J.; Wynne, K. A
Qualitative Study Supporting
factors; (iii) high symptom burden, (iv) social support impacting well-being, and (v) physical and
Optimal Nutrition in Advanced structural supports. Current screening methods do not adequately capture all potential drivers of
Liver Disease—Unlocking the malnutrition in the ALD population. Adopting a more supportive approach including both physi-
Potential for Improvement. Nutrients ological and non-physiological factors in ALD malnutrition screening may promote more timely
2024, 16, 2403. https://doi.org/ and comprehensive nutritional interventions that address the complex and holistic needs of patients
10.3390/nu16152403 living with ALD.
Academic Editor: Rosa Casas
Keywords: liver disease; malnutrition; quality of life; social support; supportive care; palliative care;
Received: 26 June 2024 screening; assessment
Revised: 18 July 2024
Accepted: 23 July 2024
Published: 24 July 2024

1. Introduction
Malnutrition in Advanced Liver Disease (ALD) is common and contributes to high
Copyright: © 2024 by the authors.
symptom burden, poorer health outcomes, increased hospital admissions, increased
Licensee MDPI, Basel, Switzerland.
This article is an open access article
healthcare costs, decreased quality of life, and increased rates of mortality [1–6]. Studies
distributed under the terms and
have shown that 20% of people living with well-compensated liver disease suffer from
conditions of the Creative Commons malnutrition, with rates increasing to 60–85% in people in advanced stages of the disease
Attribution (CC BY) license [1–3,6]. Malnutrition directly impacts severe complications of liver cirrhosis, such as asci-
(https://creativecommons.org/license tes, hepatic encephalopathy, and infections, worsening prognosis and reducing quality of
s/by/4.0/). life [6].

Nutrients 2024, 16, 2403. https://doi.org/10.3390/nu16152403 www.mdpi.com/journal/nutrients

Nutrients 2024, 16, 2403 2 of 15

Early detection and diagnosis of malnutrition is essential in ALD. The European So-
ciety for Clinical Nutrition and Metabolism (ESPEN) guidelines recommend initial screen-
ing for malnutrition using a validated tool [1–3,6,7]. While most globally used validated
screening tools seek to identify changes in dietary intake and weight, screening for mal-
nutrition in ALD can be difficult. The fluid buildup from edema and ascites may mask
weight changes, leading to inaccurate weight and body mass index calculations and
thereby decreasing the accuracy of these tools and potentially underestimating malnutri-
tion risk [6–8]. As a result, nutritional intervention is often delayed [6]. The Malnutrition
Screening Tool (MST) is an example of a screening tool commonly used in clinical practice
[3]. It is a popular tool as it is validated across multiple conditions, can be completed by
any staff member, and can be easily applied in all settings [3]. However, it is less likely to
be effective in this population as it only uses intake and weight as indicators of risk of
malnutrition [3]. Some studies have shown that in patients with cirrhosis, the MST has
poor diagnostic ability, with reduced sensitivity and lower prevalence of identified mal-
nutrition risk when compared with other screening tools [2].
The Patient-Generated Subjective Global Assessment Short Form (PG-SGA Short
Form) includes a wider range of nutritional symptoms such as nausea, taste change, and
loss of appetite, with the option to include additional factors under the category of ‘other’
[9]. However, this ‘other’ information is reliant on a patient’s health literacy or under-
standing of the condition to recognize key details to convey for effective identification and
prioritization of need [9]. Alternatively, the Royal Free Hospital-Nutrition Prioritizing
Tool (RFH-NPT) is recommended by the European Society for Enteral and Parenteral Nu-
trition (ESPEN) guidelines for malnutrition screening in patients with ALD as it is disease-
specific and considers factors beyond intake and weight [1,3]. Included in the tool are dis-
ease-related complications such as ascites and general fluid overload, therefore improving
its effectiveness for malnutrition risk detection in this population [6,10].
Non-physiological determinants such as personal, religious, and cultural values and
psychological factors play a role in malnutrition etiology but are not routinely captured
in current tools [3,6–8,11,12]. While there is limited evidence investigating the non-physi-
ological determinants of malnutrition in ALD populations, studies in other patient groups
with comparable high symptom burdens, such as oncology and renal supportive care,
have shown that incorporating these additional factors leads to more timely nutritional
intervention for those at risk of malnutrition [11,12]. This allows for better management
of symptoms, improved physical function and independence, and improved quality of
life [11,12].
Given the significant impact of malnutrition on ALD outcomes and emerging evi-
dence regarding the benefit of incorporating non-physiological determinants of malnutri-
tion in screening for ALD, a broader approach to malnutrition screening is required. The
primary aim of this research is to identify these additional non-physiological factors for
use in malnutrition screening for patients with ALD that could inform a patient-reported
screening tool. Consumer engagement explored the lived experience of nutrition concerns
in this patient group through qualitative methods. Such consumer involvement has been
shown to increase the quality, impact, and reach of clinical research [13].

2. Materials and Methods

This qualitative study is reported in accordance with the ‘Standards for Reporting
Qualitative Research (SRQR): A Synthesis of Recommendations’ [14]. Ethics approval was
provided by Hunter New England Ethics Committee reference (2022/ETH02426) on 21
December 2022. Registration was granted by the Australian New Zealand Clinical Trials
Registry (ANZCTR), ACTRN12624000472572.
Nutrients 2024, 16, 2403 3 of 15

2.1. Setting
This study was conducted within complex and supportive care liver clinics across
one metropolitan and one regional Australian public health site.

2.2. Research Steering Committee

The research team comprised a ten-member steering committee consisting of re-
searchers, doctors, nurses, and dieticians with experience in ALD. An early-career re-
search dietician skilled in working with ALD patients and supportive care convened the
research steering committee. The research dietician worked collaboratively under the
guidance of the broader research steering committee, seeking feedback and direction on
every aspect of the study design, implementation, and evaluation.

2.3. Consumer Input

For this study, it was vital to engage with a range of consumers to improve the re-
searchers’ understanding of the lived experience of malnutrition in ALD and to ensure the
richness of the data. Consumers consisted of (i) patients and (ii) carers.
Patients were eligible if they were 18 years of age or older, attended one of the liver
clinics in the research setting, were able to provide informed consent, and had Child–Pugh
B or C liver disease. As a range of lived experience was sought, current malnutrition was
not an inclusion criterion for the study; participants were invited if they had Child–Pugh
B or C status as this group would be more likely to have a current or future risk of under-
nutrition and receive dietetic input. Carers of any patient meeting the eligibility criteria
were invited to participate, with their participation dependent on receiving informed con-
sent from the patient.

2.4. Clinician Input

Dieticians, nurses, social workers, and doctors who worked across either research
site were eligible to participate. These health workers needed to be currently employed at
one of the liver clinics in the setting, caring for patients who met the eligibility criteria
and/or have experience working with the ALD population.

2.5. Recruitment
Recruitment occurred between January and March 2023. Eligible patients and carers
were identified from those who attended a clinic within the research setting. In consulta-
tion with site leads for the Department of Nutrition and Dietetics, Gastroenterology and
Supportive Care, the research dietician identified key staff members with experience in
ALD who were purposefully sampled and invited to participate. Due to a limited number
of dieticians available at the regional site, dieticians from an outlying health campus with
expertise in ALD were nominated by department leads to provide a broader range of in-
put and regional perspective. Clinicians who provided consent to participate were pro-
vided an information sheet prior to contact with the research dietician.

2.6. Data Collection

Semi-structured interviews were conducted with all consumers between January and
March 2023. Interviews were facilitated by the research dietician (blinded for peer review)
either in person, via phone, or virtually using Microsoft Teams. Interview guides were
developed to promote consistency in the data collected (see Tables 1 and 2) based on the
literature and the research team’s knowledge and clinical experience. Thirteen clinicians
were interviewed either individually or in small groups of two or three. All patients and
carers were interviewed individually.
Adroit Transcription was used to transcribe a total of eleven interviews with thirteen
participants, including two focus groups [15]. A glossary of terms was provided to tran-
scribers to give context to the interviews for more accurate transcription (see Table S1).
Nutrients 2024, 16, 2403 4 of 15

The remaining nine participant interviews were transcribed manually by the research
team due to poor recording quality. Each transcript was then checked by two members of
the research team (blinded for peer review) for accuracy.

Table 1. Interview Guide for Clinicians.

Welcome and Introductions.

Experiences of nutrition care in complex liver clinics.
• What is your experience of using nutrition screening and assessment tools in standard practice?
• Can you explain the referral processes to the dietician currently used in standard care? Can you explain how
these processes are effective or ineffective in identifying those patients requiring nutrition support?
• From your point of view, what are some of the factors influencing an ALD patient’s nutrition?
• How do current nutrition screening tools account for these factors?
• Can you explain how non-physiological factors (for example, food security, culture, dentition, psychosocial and
emotional well-being) influence nutrition for patients living with ALD?
Positive/negative comments.
• Can you explain the positive components of the nutrition screening tools currently used in standard practice?
What works well?
• Can you explain the negative components of the nutrition screening tools currently used in standard practice?
What doesn’t work well?
Feedback and suggestions for screening tool development.
• What are your suggestions on how the screening of nutrition in ALD patients could be improved?
• How could the non-physiological determinants of nutrition be incorporated into a new nutrition screening tool
for ALD patients?
• What are the main physiological and non-physiological components or considerations you think are important to
include in the novel screening tool?
General suggestions.
• Do you have any general recommendations?
• Do you have any other comments?

Table 2. Interview Guide for Patients and Carers.

Welcome and Introductions.

We know that nutrition can affect more than just your physical health. It can also be important to people’s connection
with their family, quality of life, culture and social and emotional well-being. We’d like to ask you a few questions
about nutrition, which will help us improve the way we plan and provide nutritional care.
Experiences of care.
• Can you tell me how nutrition affects your daily life?
• Other than your physical health, can you explain how nutrition impacts other areas of your well-being?
Positive/negative comments.
• What are the things that make it hard for you to have good nutrition?
• What are the things that might help you have good nutrition?
Feedback.
• What things do you think are important for the healthcare team to consider when asking about your nutrition
and how it affects your daily life?
General suggestions
• Do you have any general suggestions or comments?

2.7. Data Analysis

Transcripts were de-identified and analyzed thematically using the Braun and Clarke
method [16]. The initial coding was completed by two members of the research team
(blinded for peer review) who spent time familiarizing themselves with the transcribed
interviews by completing iterative readthroughs of each interview to gain maximum in-
sight [16]. Codes were generated for as many topics as possible, ensuring that the code
Nutrients 2024, 16, 2403 5 of 15

was not just a phrase but rather applied to a contextual segment of the interview. Two
members of the research steering committee (the dietetic honors student and one senior
research dietician) generated themes from the existing codes and sorted these into catego-
ries that best encompassed their meaning [16]. Themes were further refined during two
consultations with the broader research steering committee for review, revisiting and re-
organizing codes and subthemes until a consensus was obtained [16]. The sample size was
deemed large enough to provide adequate information power due to the narrow focus of
the study, specific sample population, and clinical expertise of the research team [17]. Sup-
porting exemplars were then extracted from the text, aiding in the refining of the names
of the themes, ensuring that they were conceptually parallel [16]. NVivo 12 software was
used to assist in the organization and visualization of the data [18].

3. Results
There was a total of twenty-two participants included in this study: eleven clinicians,
nine participants, and two carers. Five clinicians and two patients came from the regional
sites. Six clinicians, seven patients, and two carers came from the metropolitan site (see
Figure 1). Patient participants had a diagnosis of hepatitis B, hepatitis C, and/or alcoholic
liver disease and had received dietician input into their care planning during standard
care liver clinics in the six months prior to being recruited to the study. Two of these pa-
tient participants had been diagnosed with hepatocellular carcinoma, with one having
received immunotherapy. There was a 100% participation rate with all patients, carers,
and clinicians approached for the study agreeing to be interviewed. Interviews lasted be-
tween five and thirty minutes.
When exploring the factors influencing the nutritional status of the ALD population,
five main themes were identified: (i) appropriateness of healthcare delivery; (ii) health-
and food-related factors; (iii) high symptom burden, (iv) social support impacting well-
being, and (v) physical and structural supports (see Table 3 for themes, sub-themes, and
supporting quotes).

Figure 1. Flow chart for the recruitment of participants.

Nutrients 2024, 16, 2403 6 of 15

Table 3. Themes, sub-themes, and supporting quotes.

Theme Sub-Theme Demonstrative Quotes—Patient or Carer Demonstrative Quotes—Clinician

“They might have already been in the hospital for say, five days, before we
even know about them and I think that really is a reflection of the MST, not
capturing the issues that the patient has.” (clinician)
“Yeah well didn’t have the right people around her. I suppose it was month in, “If there was an effective screening tool, that would obviously create more
month off, every six weeks she’d end up in [de-identified] Hospital, um, she’d referrals to a dietician, or more appropriate referrals, potentially. What I
make little improvements, but there was no eating involved. Ah, she made know across the hospital, is a malnutrition screening tool is, not sensitive
Appropriateness Accurate
little improvements then they’d send her home. Um, and you’d just wait five enough to pick up the people who really need it or often results in multiple
of Healthcare Screening/Correct
or six days and we’re on the downhill slide again. Look, the only thing that referrals for people who don’t really need to see a dietician at all, so I think
Delivery Referrals
changed (de-identified) life was meeting that lady in the waiting room that it really needs to be developed for the population that we are looking at, at
day and getting (de-identified) in the liver clinic, or my daughter would be the time, or using something more in depth than just a MST” (clinician)
dead.” (carer) “Very difficult with weight changes-increase in ascites [and] decrease in
muscle mass.” (clinician)
“it’s just a bit of a hit and miss…it doesn’t seem to be a real clear process…
[of] who gets referred to the dietician”. (clinician)
“If I needed to ring up and ask a question about if I could eat something or
not, eat something which is great, like you guys jumped on. If you guys didn’t
know. I know you personally look up for me whether I should have it or how
much I would like to have that.” (patient)
“I was (de-identified) primary carer and the kids’ primary carer, I had
somebody…you blokes were ringing me up a couple of times per week, just to “entering a more…transient approach…being in the same room, or sharing
Supportive Care
make sure how things were going and that. Do you know how much benefit notes, getting a bigger picture of what’s happening in the world and
Team
that did for me? Do you know how much benefit that gave (de-identified)? bouncing off each other always seems to work really well.” (clinician)
Knowing somebody gave a s**t…but you blokes are liver specialists and
dieticians and doctors and…mental health person, you know she was
beautiful too. Having the right group around you, especially a group that sort
of specialises in that stuff, if you like, when no-one else really took it very
serious, so um, life changing, for both of us.” (carer)
“had to have a root canal the other week. So they’ve been pretty bad and
“We’ve had patients with dental issues that’s impacted their nutrition”
there’s more to be done there…I don’t have the money, but I don’t want to go
(clinician)
around with no teeth either.” (patient)
Health- and Food- “issues with dentition” (clinician)
Dentition “they said if you don’t…get that tooth fixed, you won’t be able to eat on that
Related Factors “changes to dentition of course changes what people can eat and what they
side of your mouth.” (patient)
can tolerate, that links in often with financial things, not being able to get
“[food] gets stuck all over my dentures…I gotta keep going to the bathroom
their teeth fixed, or access the services that they need” (clinician)
and cleaning my teeth out.” (patient)
Nutrients 2024, 16, 2403 7 of 15

“I’d say, like cooking skills and food preparation skills are, on average,
lower in this population”. (clinician)
“You know, last night I had a bit of cheese and flavoured milk and all that and “the health literacy of a lot of the patients that come to clinic and I guess…
that’s always good, you know I’ll drink flavoured milk rather than drink an it has to be balanced… a lot of patients would struggle or lose interest or
apple juice, or something like that. yeah, yeah, so good education and meal not understand.” (clinician)
Food Literacy
suggestions [would help improve nutrition]” (patient) “they’ve not had good, potentially, dietary or nutrition inputs until now
“And the goodness [they’re] getting from the food to make it worthwhile and so those [negative] habits are formed.”(clinician)
eating, hmm. Like common understanding of nutrition.” (patient) “I guess general knowledge about health because they probably, I know it’s
very stereo-typical but, um, they’ve not made positive, healthy, lifestyle
choices, so it’s hard to break that barrier as well, sometimes.” (clinician)
“I had wine and there was two and then there was three and then there was
four long drinks. I’d drink right up until news was over at 7 o’clock, cook “There can often still be alcohol consumption, which can affect their
Alcohol some dinner and have one bite and put it in the fridge, saying I’d have it nutrition.” (clinician)
Consumption tomorrow and it’d end up in the bin, so the alcohol was probably sustaining “a lot of people we do know still have a reliance on alcohol as well, which
my hunger perhaps, I don’t know, but it put me in the wrong frame of mind to can impact their nutritional status, so I guess it’s multi-factorial.” (clinician)
get some tucker in to me and feeling healthy.” (patient)
“Oh, um, well at the moment, ‘cause being sick and all that, sort of affects
[diet] probably different ways than what you’d probably expect.” (patient)
High Symptom “stage of disease [influences nutrition].” (clinician)
Sickness “it’s the absolute sickness.” (patient)
Burden “the disease state is probably a big thing, in progression.” (clinician)
“She spent more time with her head in a bucket, than she did with her head on
a pillow” (carer)
“I was eating perfectly and then one day I just decided I didn’t feel like eating
anymore and yeah food just didn’t interest me at all like nothing and it took a
Unexpected “physiological things, ascites, nausea, vomiting, poor appetite, loss of
very long time to get that interest that I wanted to eat back that’s for sure”
Symptoms taste,” (clinician)
(patient)
“I get full pretty quick.” (patient)
“And quite often when I eat I throw up. Just out of the blue. But with some “a lot of people with liver disease, their ascites can cause nausea and...
Cascade nausea in the beginning or just randomly after eating… I ate and it makes it shortness of breath and things as their ascites can build up...and impact
worse, because you’re feeling so uncomfortable.” (patient) their diet in that way and changes to their bowels.” (clinician)
“Yeah, that most people find it a really pleasurable thing whereas it’s a bit of a
chore for me [eating].” (patient) “I think, a lot of the time I think there is loss of appetite.” (clinician)
Loss of Interest in
“I do get a funny taste in my mouth…it’s like a filter’s been put over my “The ascites is when they’re really quite bloated, they find it difficult to
Food
tongue and my tastebuds. If I want to try and enjoy something and that filter’s eat.” (clinician)
over there and I can’t taste it, I think well what’s the point?” (patient)
Nutrients 2024, 16, 2403 8 of 15

“I went to the butcher today and I bought all this stuff. I thought, well I’m
really good at buying food, sometimes I’m good at preparing it, I’m just not
good at eating it” (patient)
“No appetite, like I literally have to make myself eat” (patient)
“The ascites, I think, had a lot to do with it and having the NG tube made it
harder to eat for me.” (patient)
“He’s gone off meat and everything like that, so it’s hard to get him interested
in food, to get him to eat.” (carer)
“It’s just...it’s just the energy level, I just can’t be bothered making…I bought
that Light and Easy, but I’ve gone off that, so…I really don’t know what I’m
going to do for…I just can’t be bothered, type of thing.” (patient) “people may not have always had healthy eating habits and but it’s also
“Sometimes it’s day three of diarrhea and I feel rotten, so I can plan that sort of actually identifying do they actually see that as a problem, do they want
Loss of Motivation stuff but as far as a meal goes, food goes, I, plan it but…I won’t go ahead with help with that”. (clinician)
it.” (patient) “that motivation to cook and to…actually prepare the meals can be limited
“When I’m in a care situation and food’s put in front of you…it’s easier to do as well”
that. I need to get the motivation to cook for myself and enjoy that again.”
(patient)
“When they [are] confused, they just don’t wanna eat. They get to the point
Confusion “you’re just too confused to even think about food.” (patient)
where, yeah, they just don’t wanna eat.” (clinician)
“Physically, I couldn’t walk. I literally couldn’t lift my three-month-old son up
at the time, I barely could move off the lounge. I just slept all day. I had no
energy whatsoever… I couldn’t go to the shops, I couldn’t carry any bags I “One of the key symptoms that you see from the liver clinic which probably
couldn’t take the kids to the park or out to the beach or anywhere like that 90 per cent of people experience is lethargy and so preparing something
because I physically couldn’t walk more than 5 meters” (patient) that’s nutritious and that doesn’t come out of a packet somewhere or from a
Loss of Energy “My body’s not absorbing protein so that makes me really tired and then you take-away store is…takes energy and that can steal something from their
get tired and it’s just like that wicked circle again, you get tired, you can’t be ability” (clinician)
bothered you just don’t do and I’m just trying to step over that at the moment” “Their, energy levels, and you know, um, their desire to eat and prepare
(patient) food.” (clinician)
“she didn’t have the strength, the energy, she didn’t have um, the desire.”
(carer)
“When I’m depressed I don’t eat.” (patient)
“Not having the nutrition that I needed to have, it depressed me a lot, it gave “I think sometimes some of these people, like, you’d say 80 per cent of them
Depression me depression I couldn’t even take my daughter to school, I couldn’t be there are probably depressed…and that’s got to have an impact on, on
for her year 6 formal, yeah so my family missed out on a lot with their mum I motivation.” (clinician)
guess as well like they suffered a lot for me being sick.” (patient)
Nutrients 2024, 16, 2403 9 of 15

“If you’re not eating and you’re not getting that nutrition, you’re not feeling
like wanting to do anything. And then that affects your mental health, like it’s
a you know a horrid cycle.” (patient)
“Often may have swallowing difficulties or dysphagia related to varices”
Varices
(clinician)
“I think it’s important to know their level of support, at home, like
carers…like meals on wheels, things like that, are they using any services,
“I do online shopping and I make it for a day and a time that I know that
Social Support what services are there that can help.” (clinician)
someone else is going to be here because they drop it to the door, which is
Impacting Well- Need for Support “Sometimes don’t have good support networks so not only do they often
great, but then I’ve got to get it from the door to the kitchen and I can’t make
being forget or not hear the messages being given clearly during clinic they don’t
it.” (patient)
have that network to help keep them on the right path once at home and
assist when needed/having a low health day.” (clinician)
“I was a very independent person, I did everything on my own, I never asked
for help, I was very stubborn… Whereas now, I’m like, ‘yes please, can you do
this for me’. So that’s kind of what’s changed me a lot I suppose.” (patient)
“My dad took care of me and my kids and did a lot of the grunt work for me
cause I couldn’t physically do it but he helped a lot and he helped a lot to get
me to eat, he’d get me food that I thought I’d like to eat and not forcing me but
re reassuring me that I had to eat pretty much that was the only way I was
going to get better.” (patient)
“I ended up moving me and my kids in with my dad to support me for a few
months that I couldn’t eat and couldn’t function properly and so much. So you “somehow feeling responsible for what’s happened to them and um, not
Loss of
take my kids to school and run me to the doctor appointments and things like worthy of some of the help that some people can easily access, is easily a
Independence/Chal
that because I couldn’t drive because I was so malnutrition and I was so barrier” (clinician)
lenges with
skinny.” (patient) “lack of social support…especially if they are living on their own and
Independence
“I was with the NG tube, I pretty much didn’t eat at all. He tried to get me to they’re feeling so poorly.” (clinician)
have family meals with them guys, but I’d have a mouthful and that’d be
enough. And gradually got to the point where I’d have lunch with them, and
then I would have a family dinner. But I’ll be little and then gradually got
more and more. He’d buy me vanilla slices and things like that just to try and
fatten me up a little bit and it worked and it definitely worked.” (patient)
“If I didn’t have his support too. I don’t think I would have the energy or the
will to even want to cook anything to eat or go to the shops to get anything
that I’d like, which where he would do them things for me, which helped a
lot.” (patient)
Nutrients 2024, 16, 2403 10 of 15

“I try to always have a decent tea, you know, even if I’ve eaten nothing or, you
know, rubbish, throughout the day, I will try to have like a normal tea, where
we sit down, at the table, like a family, ah, if I’m not, ah, eating, I don’t
obviously, go to the table. You know, that takes away from that family sort of
time.” (patient)
“My daughter, she cooks meals every day and she will let me go maybe one or
two days and then that’s...she’s like ‘nah, that’s it, you haven’t had this for
ages’ and I’m like ‘uh, but I don’t feel like it’ and she’ll just dish me up
something. And I will find, probably seven out of ten times, that I do eat it.”
(patient)
“I didn’t attend my grand-daughter’s um, engagement party on Saturday, just
because you know, I hadn’t been eating and also too, because I am getting “I mean there’s a big difference in the patients who have a family or you
tired because also you don’t eat so I’m ‘I’ve got to sit down, I’ve got to sit know, have a partner and ah, patients who are single, and are on their own,
Social Isolation
down’, you know I’d be forever feeling I was being that wet towel, always yeah because I think you know, a lot of the older, single men, really
hanging around, so I just said I wasn’t going to go and so I missed out on struggle.” (clinician)
that.” (patient)
“Being able to afford to eat the amount of protein or the amount of food,
you know, or get all of those medical appointments in, travel back and
forth to [regional hospital]...it’s a huge impact, out here especially.
(clinician)
Physical and “Patients can’t afford to buy the appropriate foods, at times.” (clinician)
Socioeconomic
Structural “my dad helped me financially.” (patient) “lower socioeconomic [status] as well, so financial barriers, transport
Status
Supports barriers, things like that.” (clinician)
“I think that food security is a bigger issue than we credit in a lot of
different disease groups, that for a lot of people with um, liver disease, that
could be an issue if they are no longer working, and they don’t have a huge
social network that can support them.” (clinician)
“I’m on the DSP [Disability Support Pension] … I don’t work at the moment, “They might be on a supplement here in hospital, but they simply can’t
so I don’t have that money to spend [on supplement drinks]” (patient) afford that when they go home so we’re often recommending things like up
Affording “The dieticians that say “have those pro-biotic drinks” and this, that and the and go energisers, stuff like that, that they can easily pick up at the
Nutrition other, and they’re not cheap, you know, like, I’ve got to provide for a family so supermarket that might be a bit cheaper, so financial...those factors are,
Treatment Options I try and get stuff that we can all eat and so, yep, the finances would...would huge.” (clinician)
play a part in it. You know I buy different things for the family that I wouldn’t “Socioeconomics is a big issue, you know, people being able to afford
have just for myself.” (patient) supplements.” (clinician)
Nutrients 2024, 16, 2403 11 of 15

3.1. Appropriateness of Healthcare Delivery

Timely referrals and capturing and addressing what matters most to patients and
their carers were highlighted by carers and clinicians as important factors in this study.
Patients recognized the benefit of being able to “ring up and ask a question” and carers
identified “having the right group around you, especially a group that sort of specializes
in that stuff…when no-one else really took very serious, so um, life-changing, for both of
us”. Clinicians acknowledged that it was difficult to assess malnutrition risk with weight
changes alone due to an “increase in ascites [and] decrease in muscle mass”. This high-
lighted the need for a screening tool that could screen for more symptoms specific to the
ALD population to allow for more appropriate referrals to dieticians. Clinicians identified
that the current method of screening for malnutrition was “just a bit of a hit and miss”
without “a real clear process of who gets referred to the dietician” and “not capturing the
issues that the patient has”.

3.2. Health- and Food-Related Factors

One patient identified that having a “common understanding of nutrition” would
help increase their intake as they would then be able to understand “the goodness [they’re]
getting from the food to make it worthwhile eating”. For some patients, it was recognized
by clinicians that “they’ve not had good, potentially, dietary or nutrition inputs until now
and so those [negative] habits are formed”, as well as “a lot of people we do know still
have a reliance on alcohol as well” which can then make it “hard to break that barrier as
well, sometimes.” Clinicians noted that this impeded some patients’ comprehension of the
provided education regarding how food and nutrition may impact ALD.
It was identified by a clinician that there are “multi-factorial” components that can
impact the nutrition of people with ALD. Clinicians reported the patients’ “cooking skills
and food preparation skills are, on average, lower in this population” and could adversely
affect their nutritional status. Additionally, it was recognized that aspects such as “issues
with dentition” could impact their nutritional status as it “changes what people can eat
and what they can tolerate, that links in often with financial things, not being able to get
their teeth fixed, or access the services that they need.” This comment reflects difficulties
patients have accessing public dental health services in Australia due to the associated
costs, waiting times, limited transport options, and fewer dental practitioners in rural ar-
eas [19].

3.3. High Symptom Burden

It was identified by patients, carers, and clinicians that the common physiological
symptoms associated with ALD, such as ascites, nausea, vomiting, poor appetite, and loss
of taste, could affect a patient’s ability to maintain good nutrition. This was best described
by one patient as the “absolute sickness” that would get in the way of their nutrition.
While for some patients the symptoms were unexpected without an apparent specific
cause, for others, symptom burden was recognized as being complex and often interre-
lated, causing a cascade effect on intake: “I was eating perfectly, and then one day I just
decided I didn’t feel like eating anymore” and “Quite often when I eat, I throw up. Just
out of the blue”. As a result of these symptoms, there was a loss of interest in food, making
eating more challenging and akin to an obligatory task. The motivation to eat could be
quite transient and subject to frequent changes.
For some patients, despite best intentions, the experiences of symptoms impacted
“that motivation to cook” and to “actually prepare the meals”, as highlighted by one pa-
tient after frequent bouts of diarrhea impacted their ability to proceed with planned meals.
Additionally, one clinician reported that “80 per cent of them [patients] are probably de-
pressed,” suggesting that low mood would further impact motivation and ability to look
after one’s nutrition. As a result of experiencing symptoms, patients’ reduced energy
Nutrients 2024, 16, 2403 12 of 15

levels were recognized as impacting their ability to prepare meals; this began even before
the meal preparation stages, in being able to source food from the shops and get it home.
“Physically, I couldn’t walk. I literally couldn’t lift my three-month-old son up at the time,
I barely could move off the lounge. I just slept all day”.

3.4. Social Support Affecting Well-Being

Patients, carers, and clinicians identified the significance of social support for people
living with ALD. Patients with ALD reported a loss of independence and the need for
more support from family, friends, and carers, as exemplified by one patient’s statement:
“I was a very independent person, I did everything on my own, I never asked for help, I
was very stubborn… Whereas now, I’m like, ‘yes please, can you do this for me’. So that’s
kind of what’s changed me a lot I suppose”.
However, patients also recognized that their waning interest in food sometimes led
them to decline social invitations for fear of bringing a negative atmosphere, resulting in
missed opportunities for a supportive social dining experience. One patient responded
that “I didn’t attend my grand-daughter’s um, engagement party on Saturday, just be-
cause you know, I hadn’t been eating and also too, because I am getting tired because also
you don’t eat so I’m “I’ve got to sit down, I’ve got to sit down”, you know I’d be forever
feeling I was being that wet towel, always hanging around, so I just said I wasn’t going to
go and so I missed out on that.”
Clinicians reported they noticed “a big difference in the patients who have a family,
or you know, have a partner and patients who are single and are on their own”. When
patients had a “lack of social support…especially if they are living on their own and
they’re feeling so poorly”, this would impact a patient’s ability to maintain good nutrition
due to difficulty shopping for food and preparing meals.

3.5. Physical and Structural Support

Financial concerns were raised by some patient participants, with one patient re-
sponding that “I’m on the DSP [Disability Support Pension] … I don’t work at the mo-
ment, so I don’t have that money to spend”. It was identified by clinicians that a number
of barriers could affect a patient’s ability to maintain good nutrition; these were recog-
nized as patients of “lower socioeconomic [status] as well, so financial barriers, transport
barriers, things like that”.
In the clinicians’ experiences, finance had a big impact on “being able to afford to eat
the amount of protein or the amount of food”. This was reinforced by patients when they
were required to purchase specialty items to manage their condition or when patients
were required to access nutritional support to ensure they could meet their nutritional
requirements. In some instances, clinicians stated that patients would respond “no” when
asked if they could afford to purchase nutritional supplement drinks. As a result, the die-
ticians were altering recommendations to meet the financial needs of the patients.

4. Discussion
This novel study aimed to understand the non-traditional factors influencing the nu-
tritional intake of the ALD population. Our findings highlight several barriers and non-
physiological factors not included in standard malnutrition screening tools that influence
the nutritional status of patients in this population.
Results from this study reinforce the impact of a high symptom burden in ALD on a
patient’s nutritional status. Symptoms such as ascites, nausea, vomiting, poor appetite,
loss of taste, and low energy acted as barriers to maintaining adequate nutrition. Our
study also highlighted the multifactorial nature of these symptoms in patients, which
were often linked; for example, accumulation of ascites may cause nausea, resulting in
changes to appetite and intake. This is consistent with the literature, which indicates that
up to 50% of people with ALD will experience ascites and its consequent impact on
Nutrients 2024, 16, 2403 13 of 15

nutrition, leading to heightened malnutrition rates of up to 85% in this population [1,20].

Despite these symptoms being commonly reported in our study population and consist-
ently seen in the literature, only two of the seven validated malnutrition screening tools,
the RFH-NPT and the PG-SGA Short Form, explore disease-related complications, such
as ascites or general fluid overload [6,9,20,21]. In addition, the PG-SGA Short Form in-
cludes nutritional symptoms such as nausea, taste change, and low appetite, but doesn’t
capture fluid buildup from ascites or edema [9].
Evidence in the renal and oncology literature has identified that targeting non-phys-
iological impacts can lead to better-managed symptoms and a greater quality of life
[11,12]. In Australia, the PG-SGA Short Form is often preferred in renal and oncology set-
tings. However, our study identified that patients in the ALD population have other com-
plex needs not routinely picked up by current screening tools and experience non-physi-
ological factors that impact their nutritional intake, such as financial status, level of social
support, and food literacy levels.
It was highlighted by clinicians that the current screening tools used in this setting
did not identify all factors that influenced the nutritional status of patients with ALD,
which may impact timely and appropriate referrals for those at risk of malnutrition. As
reported in the existing literature, the MST, commonly used in clinical settings, is found
to have poor accuracy compared to tools such as the RFH-NPT [3,6]. Therefore, earlier
detection and intervention for malnutrition, as recommended by the ESPEN guidelines,
is essential to improve the quality of life and reduce the mortality rate of patients with
ALD [1,6]. This study draws our attention to the importance of considering a patient-cen-
tered approach to improve outcomes and support optimal nutrition to meet the needs of
patients with ALD.
To the authors’ knowledge, this is the first exploration of malnutrition screening in
ALD encompassing the important perspectives of patients, caregivers, and clinicians uti-
lizing a collaborative and evidence-based approach with formal consumer engagement.
As a result of their experiences, this study highlights the ineffectiveness of current screen-
ing methods and the need for more comprehensive malnutrition screening. Leveraging
the consumer and clinician insights obtained in this study can inform clinical practice to-
wards malnutrition screening that is consumer-focused and considers the unique lived
experiences of this patient population. Designing effective patient-reported outcome
measures could complement anthropometric or other measures to detect sarcopenia and
biochemical methods of assessing nutritional status, for example, serum albumin level,
total cholesterol level, and peripheral lymphocyte counts or the ‘Controlling Nutritional
Status’ (CONUT) score [22]. It is important to acknowledge there was an unequal distri-
bution of participants between the metropolitan and the regional sites. While it is not an-
ticipated that this would have altered the themes identified in the study, it would be op-
timal for future research to further explore the experiences of regional and rural people
with ALD in more depth due to the known health inequalities experienced by people in
these regions [23]. This study did not include patient participants with Child–Pugh A sta-
tus, and although it is anticipated that this would not have changed our themes, this could
be another area of future study. Consideration of the health literacy of patients with ALD
and the factors that may differentially influence meal frequency or meal quality may also
benefit from future research. Additionally, while this study explored the experiences of
patients, carers, and clinicians, there was an uneven distribution in the final numbers. As
a result, there might be a lack of representation from specific groups, potentially impact-
ing the comprehensiveness of the study [24]. Respondent validation of the findings could
further support the data [24].
Future research in this area should focus on a supportive and holistic approach to
nutritional management that considers economic, environmental, and psychosocial fac-
tors. The authors plan to develop a novel screening tool for ALD that will be evaluated in
comparison to a comprehensive subjective global assessment. Furthermore, interdiscipli-
nary care planning should be engaged to harness expertise in the management of both
Nutrients 2024, 16, 2403 14 of 15

physiological and non-physiological determinants of malnutrition, which may improve

not only the nutritional status of patients but also their quality of life.

5. Conclusions
Malnutrition rates in patients with ALD are higher when compared to patients with
well-compensated liver disease. This study aimed to understand the non-traditional fac-
tors perceived to influence the nutritional status of patients with ALD which are not cur-
rently included in malnutrition screening tools. A wide range of physiological and non-
physiological factors that can affect the nutrition status of patients with ALD were identi-
fied by the diverse group of stakeholders; these warrant consideration in the development
and implementation of malnutrition screening tools for ALD. To our knowledge, no cur-
rent published screening tools consider both the physiological and non-physiological fac-
tors of malnutrition in the ALD population. Therefore, we recommend the development
of a novel screening tool that incorporates these aspects to screen for malnutrition in this
population more accurately.

Supplementary Materials: The following supporting information can be downloaded at:

https://www.mdpi.com/article/10.3390/nu16152403/s1, Table S1: Glossary of Terms.
Author Contributions: Conceptualization, S.P., J.A., and K.W.; methodology, S.L., S.P., J.A., and
K.W.; software, S.L., K.F., and S.P.; validation, S.L., S.P., J.A., and K.W.; formal analysis, S.L., K.F.,
K.S., and S.H.; investigation, S.L. and J.O.; resources, S.L., S.P., J.A., and K.W.; data curation, S.L.,
K.F., K.S., and S.H.; writing—original draft preparation, S.L., K.F., and K.S.; writing—review and
editing, S.L., K.F., K.S., S.H., J.O., S.P., J.A., and K.W.; visualization, S.L., K.F., K.S., S.H., and S.P.;
supervision, K.S., S.H., S.P., J.A., and K.W.; project administration, S.L. and K.W.; funding acquisi-
tion, K.W. All authors have read and agreed to the published version of the manuscript.
Funding: This research was supported by seed funding from the Hunter Medical Research Institute
(HMRI) Equity in Health and Wellbeing Research Program Seed Grant Scheme 2022 and the John
Hunter Hospital Charitable Trust Grant Scheme 2022 Hunter New England Local Health District
(HNELHD).
Institutional Review Board Statement: Ethics approval was granted by the Hunter New England
Human Research Ethics Committee (2022/ETH02426, 21 December 2022). Governance site-specific
approval was granted for Hunter New England (2022/STE04011, 18 January 2023; 2022/STE04012,
18 January 2023).
Informed Consent Statement: Informed consent was obtained from all subjects involved in the
study.
Data Availability Statement: The original contributions presented in the study are included in the
article/supplementary material; further inquiries can be directed to the corresponding author(s).
Acknowledgments: The authors thank Jane Kerr, Mary-Anne Dieckmann, Paulett Barnes, and all
patients, carers, and clinicians for their involvement and insights.
Conflicts of Interest: The authors declare no conflicts of interest. The funders had no role in the
design of the study; in the collection, analyses, or interpretation of data; in the writing of the manu-
script; or in the decision to publish the results.

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