Received: 20 December 2023 | Accepted: 20 April 2024

DOI: 10.1111/jhn.13315

ORIGINAL ARTICLE

Health professional attitudes and perceptions of prehabilitation

and nutrition before haematopoietic cell transplantation

Laura J. Miller1,2 | Vanessa Halliday3 | John A. Snowden4,5 |

2 5 4
Guruprasad P. Aithal | Julia Lee | Diana M. Greenfield

1
Department of Dietetics and Nutrition,
Nottingham University Hospitals NHS Trust, Abstract
Nottingham, UK Background: Nutritional prehabilitation may improve haematopoietic cell
2
School of Medicine and Population Health, transplantation (HCT) outcomes, although little evidence exists. The present
University of Sheffield, Sheffield, UK study aimed to understand healthcare professional (HCP) perceptions of
3
NIHR Nottingham Biomedical Research prehabilitation and nutritional care pre‐HCT in UK centres.
Centre, Nottingham University Hospitals NHS
Methods: An anonymous online survey (developed and refined via content
Trust and University of Nottingham,
Nottingham, UK experts and piloting) was administered via email to multidisciplinary HCPs in
4
Sheffield Teaching Hospitals NHS Foundation
39 UK adult centres, between July 2021 and June 2022. Data are presented as
Trust, Sheffield, UK proportions of responses. Routine provision denotes that care was provided
5
British Society of Blood and Marrow >70% of time.
Transplantation & Cellular Therapy Results: Seventy‐seven percent (n = 66) of HCPs, representing 61.5%
(BSBMTCT), London, UK (n = 24) of UK adult HCT centres, responded. All HCPs supported
prehabilitation, proposing feasible implementation between induction
Correspondence
chemotherapy (60.4%; n = 40) and first HCT clinic (83.3%; n = 55). Only
Laura J. Miller, Department of Dietetics and
Nutrition, Nottingham University Hospitals 12.5% (n = 3) of centres had a dedicated prehabilitation service. Nutrition
NHS Trust, Nottingham City Hospital, (87.9%; n = 58), emotional wellbeing (92.4%; n = 61) and exercise (81.8%;
Hucknall Rd, Nottingham, NG5 1PB, UK. n = 54) were considered very important constituents. HCPs within half of
Email: laura.miller44@nhs.net
the HCT centres (n = 12 centres) reported routine use of nutrition screening
Funding information pre‐HCT with a validated tool; 66.7% of HCPs (n = 36) reported using the
None malnutrition universal screening tool (MUST). Sixty‐two percent (n = 41)
of HCPs reported those at risk, received nutritional assessments,
predominantly by dietitians (91.6%; n = 22) using the dietetic care process
(58.3%; n = 14). Body mass index (BMI) was the most frequently reported
body composition measure used by HCPs (70.2%, n = 33). Of 59
respondents, non‐dietitians most routinely provided dietary advice pre‐
HCT (82.4%; n = 28 vs. 68%; n = 17, p = 0.2); including high‐energy/protein/
fat and neutropenic diet advice. Prophylactic enteral feeding pre‐HCT was
rare, indicated by low BMI and significant unintentional weight loss. Just
under half (n = 25 of 59, 42.4%) HCPs reported exercise advice was given
routinely pre‐HCT.
Conclusions: Nutrition and prehabilitation pre‐HCT are considered important
and deliverable by HCPs, but current provision in UK centres is limited and
inconsistent.

KEYWORDS
diet, haematopoietic cell transplantation, malnutrition, nutrition, prehabilitation, rehabilitation

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided
the original work is properly cited.
© 2024 The Authors. Journal of Human Nutrition and Dietetics published by John Wiley & Sons Ltd on behalf of British Dietetic Association.

J Hum Nutr Diet. 2024;1–15. wileyonlinelibrary.com/journal/jhn | 1

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2 | HEALTH PROFESSIONAL ATTITUDES BEFORE HCT

Key Points
• Prehabilitation was considered important in the context of haematopoietic
stem cell transplantation care by all health care professionals (HCPs),
although only 12.5% of centres had a dedicated prehabilitation service.
• There are inequities in nutritional care provision prior to haematopoietic
cell transplantation (HCT) between transplantation centres.
• Lack of nutrition screening and systematic approaches to body composition
assessments may limit the potential to identify and optimise nutritional and
functional health prior to HCT.
• Non‐dietitians most frequently provided dietary advice pre‐HCT. Dietary
advice focused on total energy intake (71.1%, n = 32) over protein (46.7%,
n = 21), fat (44.4%, n = 20) and fibre (24.4%, n = 11).

INTRODUCTION These nutritional sequelae both precede and

transcend the HCT process, exacerbated by previous
Haematopoietic cell transplantation (HCT) is a procedure treatments, side‐effects and complications of HCT
used to treat malignant and non‐malignant haematological such as nutrition impact symptoms and GvHD.
disorders. In 2019, primary indications for HCT in centres Following HCT, there is also an increased risk of
reporting to the European Society of Blood and Marrow further nutrition related comorbidities such as meta-
Transplantation (EBMT) were haematological malignancies bolic syndrome and diabetes, 6,13 which can develop as
(88.7%, n = 38,659), followed by non‐malignant haematolo- a late effect. 14,15
gical conditions (3.9%, n = 1691), solid tumours (3.6%, Despite the potential impact of nutrition sequelae
n = 1576), immunological disorders (3.0%, n = 1292) and on HCT outcomes, a survey of European HCT
‘other’ indications (0.8%, n = 363).1 For those recipients with centres16 showed nutrition practices were inconsistent
a cancer diagnosis, most will have received numerous cycles and failed to meet international guidelines. 17 Along-
of varying intensity chemotherapy regimens prior to HCT to side this, although international accreditation stan-
control disease, which may result in an associated risk of dards for HCT in the USA and Europe recommend
deconditioning events. having access to some allied services, they do not
The HCT process itself is physically and emotionally stipulate definitive need for dietetic support of
demanding, negatively impacting the nutritional,2,3 patients.18
functional4 and psychological status5 of recipients. Intervening early with proactive nutritional care
Patients are treated with high dose cytotoxic therapy may help mitigate some of these risks and contribute
(chemotherapy ± total body irradiation) with the aim of to improved HCT outcomes. The UK National
destroying diseased cells. An infusion of stem cells is then Health Service (NHS) long‐term plan calls for
given, which engraft and differentiate into mature personalised19 proactive20 interventions that enable
functioning cells of the blood and immune system, such self‐management.21 Prehabilitation is a package of
that the disease indication enters remission and is proactive interventions aiming to optimise physical
potentially cured. The type of HCT depends on whether (including nutritional) and emotional wellbeing
the infused stem cells are collected from the individual before treatment, through the identification of deficits
(autologous transplant) or from a donor (allogeneic and delivery of personalised intervention(s). 22 There
transplant). Allogeneic transplants are associated with are numerous population specific definitions for
greater complications and longer recovery than autolo- prehabilitation, such as the definition by Silver and
gous transplantation.6 Baima 22 for cancer: “a process on the cancer
Nutritional sequelae such as obesity, malnutrition continuum of care that occurs between the time of
and sarcopenia impact and predict HCT outcomes. cancer diagnosis and the beginning of acute treatment
Obesity pre‐HCT is increasingly prevalent7 negatively including assessment of baseline function, identifica-
predicting 100‐day readmission, nonrelapse mortality8,9 tion of impairments, and provision of interventions
and Graft‐versus‐Host Disease (GvHD) rates.8 Mal- that promote health in order to reduce the incidence
nutrition, defined as undernutrition in this context, and/or severity of future impairments”. These defini-
impacts treatment outcome, length of admissions, infec- tions can help to characterise programme aims,
tious complications,9 fatigue and quality of life.10 context and constituents, informing research, policy
Additionally, secondary sarcopenia, a loss of skeletal and clinical service delivery.
muscle mass associated with cancer related inflammation Surgical prehabilitation programmes have been
and nutritional deficiencies,11 is an independent negative shown to reduce hospital length of stay, infection
prognostic indicator for HCT outcomes.12 rates and improve quality of life.23 This has led to
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MILLER ET AL.
| 3

increasing interest in its potential role in haematolo- January 2022. Online consent was taken as part of the
gical settings; however, few studies of prehabilitation questionnaire, and all responses were anonymous.
in HCT exist. 24 Additionally, nutrition interventions
within prehabilitation studies have been shown to
vary, lack detailed description and are often poorly Data analysis
evaluated.25 Despite the expansion of prehabilitation
services to HCT settings, the prehabilitation services Responses were downloaded from REDCap cloud to
currently being delivered in the UK, nutrition Excel 365, version 2312 (Microsoft Corp.). Incomplete
practices pre‐HCT and the feasibility of nutritional and duplicate entries were removed. Quantitative data
prehabilitation in this context are all poorly were imported to SPSS, version 29 (IBM Corp.) for
understood. analysis. Proportions of respondents for each item were
The present study aimed to explore the current reported (%, n). When reporting prehabilitation or
provision and healthcare professional (HCP) perceptions nutritional practices within a centre the average response
of prehabilitation and nutritional care pre‐HCT within for all HCPs within a centre were used. Provider of
UK and Republic of Ireland HCT centres. Definitions of dietary advice delivered was dichotomised into dietitians
prehabilitation in the context of HCT, perceptions on its and non‐dietitians to review differences in advice by
implementation, and nutrition practices such as screen- HCPs. Because of the small sample, size correlations
ing, assessment and intervention delivery were also were not considered. Thematic analysis28 was used for
investigated. qualitative free text question data, initial analyses were
conducted by one of the investigators (LJM) and
reviewed by another (DG) with discrepancies reviewed,
METHODS discussed and agreed.

Questionnaire development and piloting

Ethical statement
The questionnaire was developed by six content experts
covering nutrition and metabolism, prehabilitation and The study was registered with the Health Research
HCT. Questionnaire contents were informed by pre- Authority who confirmed that ethics approval was not
habilitation guidelines,26 nutrition practices in HCT3,17 required. All local governance and GDPR processes were
and similar studies in other cohorts.16 Question and followed. Clinicaltrials.gov: NCT05352789.
answer constructs were reviewed by experts and rationale
for both questions and wording was discussed.27
Amendments were made and the full questionnaire RESULTS
piloted by five HCPs for feedback, which was then
incorporated into a definitive version. A range of Respondent characteristics
question types including five‐point Likert scale, multiple
response and open‐ended questions were included. Ninety‐nine responses were received, 23 were excluded as
Participants were also presented with the definition of a result of no parts of the consent or survey being
prehabilitation by Silver and Baima22 to consider its completed. This left 66 unique respondents, from 24
relevance for the context of prehabilitation in HCT. transplant centres, with responding centres covering
Great Britain and Republic of Ireland, and no Northern
Irish centres responding. Most respondents were dieti-
Dissemination and data collection tians (39.4%, n = 26) (84.6%, n = 22; haematology spe-
cialist dietitians), followed by haematologists (21.2%,
The survey was imported onto REDCap Cloud, version n = 14) and nurses (25.8%, n = 17)). Other staff included
1.4 (https://www.redcapcloud.com) and distributed via physiotherapist (6.1%, n = 4), occupational therapist
email by the British Society of Blood and Marrow (3%, n = 2), HCT coordinators (3%, n = 2) and one
Transplantation and Cellular Therapy to clinical leads at clinical psychologist (1.5%). Most respondents (80.3%,
39 adult HCT centres between August 2020 and n = 53) reported they delivered clinical care pre‐HCT.
February 2022. The questionnaire was also disseminated Responses were received from HCPs in 24 HCT
via email to dietetic departments within centres. Invita- centres (61.5% of target), 75% (n = 18) of centres
tion emails included a summary of the study and the represented by the HCP respondents delivered both
participant information sheet. No data or precedents on autologous and allogeneic HCT with an average of 152
sample size were available; therefore, a pragmatic multi- (72–240) transplants per year, and 25% (n = 6) delivered
disciplinary recruitment target of one nurse, dietitian and autologous only, with an average of 39 (12–70)
doctor from each centre was determined. Three email transplants per year. Respondent and centre character-
reminders were sent in September 2020, July 2021 and istics are provided in Table 1.
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4 | HEALTH PROFESSIONAL ATTITUDES BEFORE HCT

T A B L E 1 Respondent characteristics and that of their associated HCT prehabilitation provision

transplant centres.

Healthcare professional (HCP) (N = 66) N (%) HCPs within only three centres (12.5%) showed agreement
on the provision of a dedicated multidisciplinary prehabilita-
Profession
tion service for HCT in their centre. In some centres, there
Dietitian (N = 26; 39.4) was disagreement between HCPs on whether dedicated
Haematology specialist 22 (33.3) prehabilitation was provided or not (16.7%, n = 4), with
4.2% (n = 1) reporting that they were unsure. Potential
Nonspecialist 4 (6.1) reported explanations for this included nurse led prehabilita-
Nurse (N = 17; 25.7) tion with option to refer into support services such as
dietetics, but no dedicated prehabilitation capacity.
Clinical nurse specialist 14 (21.2)

Nurse (other) 3 (4.5)

Doctor (N = 14; 21.2) Defining prehabilitation in the context of HCT

Haematologist (consultant) 14 (21.2)
When asked to consider the definition of prehabilitation by
Haematology (doctor other) 0 Silver and Baima22 in the context of HCT, 57.6% (n = 38) of
Allied health professional (N = 7; 10.6) HCPs felt the current definition could be applied to HCT
without modification. However, 21.2% (n = 14) felt modifi-
Physiotherapist 4 (6.1) cations were required and 18.2% (n = 12) were unsure; 50%
Occupational therapist 2 (3) (n = 6) of which went on to suggest modifications. Further
details of HCP suggested changes are provided in Table 2.
Psychologist 1 (1.5)
Themes derived from these suggestions were then used to
Bone marrow transplant coordinator 2 (3) inform a HCT‐specific refinement of the definition by Silver
Proportion delivering clinical care pre‐HCT 53 (80.3) and Baima.22
Haematopoietic cell transplant centre (N = 23) N (%)

Treated populations in adult centres Proposed definition of prehabilitation in HCT by

≥18 years 15 (65.2) Miller et al.
≥16 years 8 (34.8) “Prehabilitation is part of a proactive multiphasic
Combined adult/paediatric unit 7 (30.4) rehabilitation continuum, involving early assessment of
baseline function (screening), identification of impair-
Combined adult/teenage and young adults' unit 9 (39.1)
ments (assessment), and provision of interventions that
Locality of centres promote physical and psychological wellbeing prior to
Northern England 4 (17.4) HCT. It is a personalised holistic process that empowers
recipients and families via multidisciplinary expert
Midlands 4 (17.4)
guidance with the aim of reducing the incidence and/or
Eastern England 1 (4.3) severity of future impairments”.
Southern England 5 (21.7)

London 4 (17.4) Implementation of prehabilitation in HCT

Scotland 2 (8.7)

Wales 1 (4.3)
Timing
Northern Ireland 0 All respondents felt prehabilitation should be considered
Republic of Ireland 2 (8.7) as part of future HCT services. Most (83.3%, n = 55) felt
this could be implemented in the pre‐HCT assessment
JACIE accredited centres
clinic; for example, end of consolidation chemotherapy
Initial accreditation 2 (8.7) or other treatment. However, 60.6% (n = 40) felt pre-
Re‐accredited 12(52.2) habilitation could be delivered either during or at the end
of induction chemotherapy before consolidation chemo-
Not accredited 9 (39.1) therapy, with 10.6% (n = 7) suggesting delivery at the
Abbreviation: JACIE, Joint Accreditation Committee ISCT‐Europe point of diagnosis. Figure 1 shows prehabilitation timing
& EBMT. perspectives of dietitians' and non‐dietitians.
 MILLER
ET AL.

TABLE 2 Template analysis of proposed definition modifications for haematopoietic cell transplantation (HCT) relevance.

Total number of
Theme Subtheme respondentsa (N = 20) Selection of exemplar quotesb Respondent (identifier)

Timing Acute episode 10 “There is very little time between diagnosis and treatment for acute haematology patients – would Nurse (7)
be better to undertake prehab during induction chemo and prior to HCT”

“Patient prehab for BMT are often already on active/acute treatment (chemo) so the definition Dietitian (9)
should be amended to incorporate this, for example time of decision for a BMT and admission
for BMT”

“In case of urgent treatment it may not always be possible to intervene before first line treatment Dietitian (16)
so it may be able mitigating losses than optimisation”

Multiphasic treatment 6 “There are multiple acute phases of treatment in cancer treatment over a life course” Dietitian (1)

“assessment on a continuum” Nurse (15)

“Needs change in relation to the fact that there is no real time between diagnosis and treatment so Dietitian (13)
needs to be assessed on treatment then again Pre Tx”

“timing of intervention can be different depending on previous acute treatment” Physiotherapist (18)

Population Inclusivity 3 “Does not account for transplant in non‐malignant conditions, that is MS, sickle cell disease, Nurse (17)
aplastic anaemia”

“Some HCT patients do not have a cancer diagnosis” Physiotherapist (12)

HCT selection 2 “It is a very good definition, but it does not support the idea of utilising in patient selection for Nurse (3)
transplant”

“May not be a plan for HCT at the time of diagnosis” Dietitian (8)

Delivery MDT 3 “Add in how it is the job of the whole MDT to provide prehabilitation, an opportunity for Dietitian (5)
specialists to contribute”

“physical and psychological” Nurse (4)

Programme constituents 4 “It is aspirational but doesn't define what should be implemented” Consultant (6)

“it is important to outline within prehab expectations, goals and what alternative methods are Dietitian (11)
needed to reach these”

Abbreviations: BMT, bone marrow transplant; HCT, haematpoietic cell transplantation; MDT, multidisciplinary team; MS, multiple scelerosis; Prehab, prehabilitat; Tx, treatment.
a
The total number of respondents relates to the number of contributing comments related to the theme;
b
The exemplar statements provided are indicative of the comments provided by the participants relevant to the theme but do not include all responses.
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6 | HEALTH PROFESSIONAL ATTITUDES BEFORE HCT

F I G U R E 1 When in the haematopoietic cell transplantation (HCT) pathway do you think a prehabilitation service could be introduced? In the
context of those with a malignancy.

Prehabilitation components Nutritional care pre‐HCT

Emotional wellbeing (92.4%, n = 61), nutrition Nutrition screening
(87.9%, n = 58) and physical activity (81.8%, n = 54)
in prehabilitation were considered very important. Respondents identified that 50% (n = 12) of the 24
Additional constituents proposed in free text centres nutritionally screened recipients using a
responses, included social and financial advice, validated tool >70% of the time pre‐HCT. Barriers
fatigue management, medication optimisation, and to nutritional screening were reported by 61 respon-
the incorporation of family and friends in prehabili- dents (92.4%). This included available time (50%,
tation delivery. n = 33), training (34.8%, n = 23), staffing (54.5%,
n = 36), anthropometric measuring equipment
(12.1%, n = 8), information communications technol-
Barriers and facilitators ogy (i.e., ICT) equipment (12.1%, n = 8) and clinic
space (31.8%, n = 21). Of those HCPs reporting
Just under half of respondents (45.5%, n = 30) felt there nutrition screening was completed (n = 56) the Mal-
were no barriers to prehabilitation delivery in HCT. nutrition Universal Screening Tool (MUST) (66.7%,
Where barriers were identified (54.5%, n = 36), the most n = 36) was the most widely used. If a patient were
common were staffing (61.1%, n = 22) and funding (41.7%, identified as at risk of malnutrition during screening,
n = 15). Table 3 provides themes of barriers and facilita- 79.4% (n = 54) of respondents advised they had a
tors taken from free text quotes by HCP respondents. dietetic service they could refer to.
 MILLER

TABLE 3 Respondent perceptions on potential barriers to prehab in UK haematopoietic cell transplantation (HCT) centres.
ET AL.

Total number of
Theme Subtheme respondentsa (N = 36) Selection of exemplar quotesb Respondent (identifier)

Staffing Provision 18 “Lack of staffing, provision, and resources within therapies to provide a prehabilitation service. My Dietitian (2)
concerns would be time taken away from inpatient work unless it was properly funded”

“Availability of professionals to complete it” Haematologist (27)

“Resources. We try our best but as our dietetic resources are spread across haematology, oncology and Dietitian (23)
HCT we find it very difficult to see patients and implement plans prior to HCTs”

“Hard for smaller centres to implement with limited staffing. Likely more relevant to allogeneic transplant” Haematologist (21)

Skill mix 3 “My concern prehabilitation will be delivered by specialist nurses rather than using clinical AHP specialists Haematologist (8)
such as dietitians and physiotherapists”

“A dedicated AHP team is required in order to delivery this service effectively, to ensure pre and Occupational Therapist (13)
rehabilitation needs are met”

“For optimum quality and pt benefit, I would prefer it to be provided by haematology dietitians for Physiotherapist (35)
haematology patients rather than generic “cancer” pre‐hab which is often based on solid tumours and
often for surgical pathways – very different needs often”

Training 3 “Appropriately trained individuals to deliver the same” Haematologist (16)

“The service should be delivered by competent staff could be an issue. The staff should be appropriately Dietitian (28)
trained”

Funding 14 “My concern would be a lack of staff and therapy resources to be able to implement a prehabilitation clinic. Nurse (1)
(Unless the appropriate and additional funding is provided)”

“Funding to support a prehab programme would be the main concern & barrier” Nurse (11)

“Current funding is not substantive for dietetics & physio, so could be lost in 2021. It is also in pilot phase, Dietitian (14)
so not embedded into all management pathways. This would require more than current available
capacity”

“Dedicated funding pathways or appropriately trained individuals to deliver the same” Haematologist (16)

Delivery 4 “Timing of initiative, patients are referred from multiple centres so difficult to find a good time to offer them Physiotherapist (5)
prehab as they are going through other aggressive treatments”

“Information overload!” Haematologist (17)

“Concerns as some patients travel a distance and would not be able to easily attend a local program” Dietitian (18)

Abbreviations: AHP, allied health professional; MDT, multidisciplinary team.

a
The total no. respondents relates to the number of contributing comments related to the theme;
b
The exemplar statements provided are indicative of the comments provided by the participants relevant to the theme but do not include all responses.
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8 | HEALTH PROFESSIONAL ATTITUDES BEFORE HCT

Nutrition assessment pre‐HCT than dietitians (40.7%, n = 11). This differed,

however, when those who had been identified as at
If the screening tool assessed someone as at risk, 61% nutritional risk (clinically or via a screening tool) were
(n = 41) of respondents reported that patients would considered with both non‐dietitians (69.2%, n = 27) and
have a nutritional assessment by a trained profes- dietitians (74.1%, n = 20) reporting similar likelihood of
sional >70% of the time. Most nutritional assessments routine (>70% of time) dietary advice pre‐HCT.
within centres were conducted using the dietetic care Forty‐five respondents (68.2%) reported they
process29 (34.1%, n = 14). Less frequently reported provided dietary advice pre‐HCT, accounting for
processes were patient generated subjective global 70% (n = 28) of non‐dietitians and 65.3% (n = 17) of
assessment (2.4%, n = 1) and handgrip strength (4.8%, dietitians. When asked how often they “individua-
n = 2), a measure of function. MUST (12.2%, n = 5) lised” this dietary advice based on clinical circum-
was reported as an assessment technique in the stances or preferences over delivery of generic advice,
“other” response options by some respondents. 44 HCPs responded. Of the 44 respondents, all
Dietitians most commonly (91.6%, n = 22) conducted dietitians (100%, n = 17) reported the personalisation
assessments within centres. Handgrip strength, a of dietary advice >70% of the time compared to non‐
measure of physical function was reported to be used dietitians (59.3%, n = 16). Information used for
as part of nutritional assessments by 32.2% (n = 19) of personalisation of dietary advice is available in the
59 respondents. Supporting information (Table S1).
Of the 45 HCPs who reported they provided
dietary advice, 71.1% (n = 32) reported giving dietary
Biochemical monitoring advice on total energy intake, 46.7% (n = 21) on
protein, 44.4% (n = 20) on fat and 24.4% (n = 11) on
Respondents (87.9%, n = 58) reported liver (86.2%, n = 50) fibre. Where respondents provided advice, there were
and kidney function (86.2%, n = 50) alongside blood pressure variations by profession (Figure 2) but the most
(79.3%, n = 46) were routinely checked >70% of the time pre‐ common patterns of dietary advice pre‐HCT were
HCT. Blood glucose (46.5%, n = 27) and lipid (32.8%, high‐protein, high‐energy, high‐fat and moderate
n = 19) levels were not routinely collected. Where samples fibre. The type of advice given by dietitians and
were collected, only 12.1% (n = 8) were reported to be fasted; non‐dietitians is provided in the Supporting informa-
however, 45.5% (n = 30) felt that fasted samples could be tion (Figure S2a–d).
facilitated. Details of HCP perceived frequency of bio- Sixty‐one HCPs reported types of specialist dietary
chemical and nutritional systemic measures taken pre‐HCT advice they gave, with just over half providing neutropenic
are provided in the Supporting information (Figure S1). dietary advice pre‐HCT (54.3%, n = 19, non‐dietitians vs.
61.5%, n = 16, dietitians). Provision of probiotic (14.3%,
n = 5 non‐dietitians vs. 34.6%, n = 9 dietitians) and prebiotic
Body composition assessment advice (2.9%, n = 1 non‐dietitian; 15.4%, n = 4 dietitians)
was less frequent and varied between dietitians and non‐
Body composition pre‐HCT was reported to be measured dietitians (see Supporting information, Table S2). Half of
>70% of the time by 45.8% (n = 27) of respondents (n = 59). the respondents did not discuss micronutrients pre‐HCT;
Methods of body composition were reported by 43 (65.1%) where they were discussed, vitamin D was the most
respondents. Body mass index (BMI) (70.2%, n = 33) was the frequently advised on (17.1%, n = 6 non‐dietitians vs.
most common. More comprehensive methods such as triceps 38.5%, n = 10 dietitians). However, advice on vitamin and
skin fold (4.3%, n = 2), mid upper arm circumference (6.4%, mineral supplementation was given more frequently by
n = 3), waist circumference (2.1%, n = 1) and bioelectrical dietitians than non‐dietitians (see Supporting information,
impedance analysis (2.1%, n = 1) were rarely used and 12.8% Table S3).
(n = 6) did not know. Haematology specialist dietitians were
most likely to be reported to conduct body composition
measurements (39.7%, n = 23 of 58). Of 61 respondents, Enteral feeding provision
BMI was felt to be most feasible in practice (82%, n = 50).
However, 86.9% (n = 53) of HCPs felt centres had the Of sixty‐one HCPs, just over one‐third (35.9%, n = 14,
equipment to conduct an alternative body composition non‐dietitians vs. 44.4%, n = 12, dietitians) reported the
measure to BMI. prophylactic placement of enteral feeding tubes pre‐
HCT. Where used, nasogastric (39.3%, n = 24) or
nasojejunal (21.3%, n = 13) feeding tubes were the
Dietary advice provision most frequently reported (see Supporting information,
Table S4). The most common reported indications for
More non‐dietitians (64.1%, n = 25) reported that all patients prophylactic tube placement were BMI ≤ 17.5 kg/m2
would receive routine (>70% of time) dietary advice (26.2%, n = 16), 10% weight loss in 6 months (21.3%,
 1365277x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jhn.13315 by Nat Prov Indonesia, Wiley Online Library on [30/06/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
MILLER ET AL.
| 9

FIGURE 2 Types of dietary advice given by healthcare professionals (HCPs) pre‐haematopoietic cell transplantation (HCT) (N = 45).

n = 13) and BMI 17.5–19.5 kg/m2 (19.7%, n = 12) (see Defining prehabilitation in HCT
Supporting information, Table S5).
HCP perceptions on definitions for prehabilitation in the
context of HCT have not previously been considered.
Exercise advice provision Because 92.3%1 of European HCT recipients will have a
cancer diagnoses, the cancer prehabilitation definition by
Of fifty‐nine HCPs, less than half (n = 25, 42.4%) reported Silver and Baima22 was reviewed by HCPs for relevance
patients would receive physical activity advice as part of to HCT. Half the respondents reporting this definition
routine practice (>70% of time) pre‐HCT. More specifically, could be directly translatable to HCT despite referring to
13.6% (n = 8) reported exercise advice pre‐HCT was given all cancer. A further one‐third felt it needed refinement to
the time, 28.8% (n = 17) often, 25.4% (n = 15) sometimes, reflect the multiphasic treatment cycles pre‐HCT, poten-
16.9% (n = 10) rarely and 15.2% (n = 9) never. Most HCPs tial acute presentation, non‐malignant presentations,
(76.9%, n = 30) reported that activity levels were rarely or short lead in times and constituents considered important
never measured pre‐HCT by questionnaire or physical to future programmes.
assessment. In the proposed Miller et al., definition, physical
wellbeing refers to nutritional adequacy, functional
fitness, and appropriate management of side‐effects to
DISCUSSION support activities of daily living. This may require a
range of supportive interventions, for example nutri-
This is the first UK survey to investigate HCP tional care,17,30 physical activity,31 social support32
reported provision of prehabilitation and nutritional (finance, carer support) and medical optimisation. In
care pre‐HCT. The findings highlight limited access to this definition, psychological wellbeing refers to a
prehabilitation within centres, no standardisation of person's ability to be aware, manage and express their
the constituents delivered and variable nutrition emotions in a way that improves life satisfaction,
provision. Yet the value of both prehabilitation and meaning and purpose and minimise the impact on their
nutrition was well recognised by HCPs. health outcomes. Strategies to support emotional
 1365277x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jhn.13315 by Nat Prov Indonesia, Wiley Online Library on [30/06/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
10 | HEALTH PROFESSIONAL ATTITUDES BEFORE HCT

well‐being may include self‐help programmes, resources prehabilitation in neo‐adjuvant chemotherapy (three to
or talking therapies (cognitive behavioural therapy33 or six cycles) with its slightly longer 3–6 weeks of pre‐
acceptance and commitment therapy34) facilitated by an operative cellular recovery37,38 but evidence with respect
appropriately qualified person. to this is also lacking.26,39
Prehabilitation constituents, such as nutrition, emo- More than 80% of respondents felt prehabilitation
tional wellbeing, and physical activity were considered was deliverable between the end of consolidation
important by HCPs, as per other guidelines.17,26 Addi- treatment and admission for HCT (approximately
tional, aspects such as multidisciplinary delivery, social 2–4 weeks), with 60.6% feeling earlier initiation at the
and financial support, fatigue management and carer end of first cycle of chemotherapy or at decision for HCT
support were identified as important considerations for was possible. This reflects cyclical (multiphasic) provi-
HCT. However, each prehabilitation programme will sion through chemotherapy/treatment prior to HCT,
need to be personalised based on the person's diagnosis, comprised of both prehabilitation and rehabilitation40,41
circumstances, type of transplantation and any prior (Figure 3). Currently published protocols for prehabili-
deconditioning leading up to HCT. Although the tation trials in HCT report intervention windows as
proposed definition by Miller et al. is informed by either pre‐HCT only42–46 or on a continuum (pre, peri
HCP perceptions of prehabilitation programme require- and post),46 with only one including personalised
ments, further refinement with those with lived experi- nutrition.43
ence is recommended.

Nutritional care pre‐HCT

Delivering prehabilitation
The impact of obesity, malnutrition, and secondary
Our capacity to understand optimal intervention, con- sarcopenia on HCT outcomes3,8,12,47 is well recognised.
stituents, duration, intensity and timing of prehabilita- However, the implementation of nutritional practices
tion programmes is limited by low‐quality heterogenous that support the identification and management of these
prehabilitation studies25,35 and limited evidence in HCT. risks was variable. Malnutrition screening is a systematic
Elective surgical prehabilitation programmes are mainly approach used to identify those at nutritional risk,
delivered in the context of de novo treatment, which is not quickly and cost efficiently at scale. Although consensus
reflective of HCT pathways. More than 80% of HCT is lacking on the optimal approach,17 early screening for
recipients receive up to three cycles of chemotherapy36 malnutrition is recommended17,48,49 preferentially with a
with 2–4 weeks of cellular recovery pre‐HCT. As such, validated measure50; however, only 50% of UK centres
HCT may have greater similarities to, and learning from, screened pre‐HCT using a validated tool (e.g., MUST).

F I G U R E 3 Example pathway for people with haematological cancer reflecting the potential impacts of multicycle chemotherapy prior to
haematopoietic cell transplantation (HCT) and prehabilitation/rehabilitation considerations at each stage.
 1365277x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jhn.13315 by Nat Prov Indonesia, Wiley Online Library on [30/06/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
MILLER ET AL.
| 11

This compares to 57% of European Bone Marrow designed in the context of frailty and ageing62
Transplant (EBMT) centres, with only 16% using a (primary sarcopenia) and not cancer (secondary
validated tool.16 sarcopenia11). These screening measures often incor-
For those identified as at risk of malnutrition porate measure(s) of function, rather than a discrete
during screening a more comprehensive assessment measure of low muscle mass. An example is the
(e.g., Dietetic Care Process or Subjective Global Strength, assistance with walking, rising from a chair,
Assessment) is then recommended. 17 The Global climbing stairs, and falls (SARC‐F) six‐item ques-
Leader's Initiative in Malnutrition (i.e., GLIM) tionnaire 63 or its derivatives (e.g., SARC‐F–calf64
published an evidence‐based framework for the [SARC‐F plus calf circumference] and the paediatric
diagnosis and grading of malnutrition in adults50 SARC‐F [PED‐SARC‐F]65 ). SARC‐F‐calf has shown
and this includes approaches for assessment. Five good predictive potential64 for low muscle mass in
core diagnostic criteria were identified: three etiolo- other cancer cohorts; however, further studies in HCT
gical (nonvolitional weight loss, low body mass index and within discrete populations (<60 years, ethnicity
(BMI), reduced muscle mass) and two phenotypic and BMI) are needed. Handgrip strength, can be used
(reduced food intake or assimilation and disease as a simple indirect or predictive measure of sarcope-
burden/inflammation).50 nia 66 and malnutrition risk,67 but small samples and
Weight and height were the most routinely reported heterogeneity in procedural reporting limits compari-
measures to be collected prior to HCT. Non‐volitional sons between studies.68 Calf circumference could also
(unintentional) weight loss of more than 10% prior to offer an alternative indicator of low muscle mass69,70
HCT may be associated with poor treatment outcomes,51 and malnutrition. 71 Procedural recommendations
with impact varying dependant on diagnosis and type of include direct skin measures, and so there may be
transplantation.52 practical limitations as to where and how calf
Body composition also impacts HCT outcomes53 but circumference may be collected in a clinic setting.
there is a lack of standardised methodology between Less than half of the HCPs in centres reported
studies54 on optimal approaches to measurements. routine provision of exercise advice and even less
Within this study, BMI was reported as the most feasible reported routine assessment of physical activity pre‐
measure of body composition to be collected prior to HCT. However, the target audience for this survey
HCT by HCPs. However, used alone, this significantly were nurses, medics and dietitians because of its
underestimates incidence of malnutrition compared to nutritional focus, and so this may reflect a lack of
validated tools, particularly in people with obesity.55 awareness or physiotherapist representation in the
Alongside this, BMI does not differentiate between fat survey, such that further investigation is warranted.
and fat free mass, where people of any weight and age Provision of dietary advice was interdisciplinary, and
can be sarcopenic (low muscle mass).30 UK HCPs rarely the level of personalisation delivered was determined by
used comprehensive measures (e.g., computed tomogra- the profession delivering the advice. HCPs reported that
phy, dual energy X‐ray absorptiometry or bioelectrical dietary advice pre‐HCT focused on total energy needs
impedance analysis) of body composition, limiting the and high‐fat dietary advice, with only one‐third advising
potential to identify low muscle mass in practice. These on protein and even less on fibre. This type of advice has
approaches also allow monitoring of changes in fat mass, potential limitations; for example, the optimisation of
which have been shown to increase during HCT.56 The muscle mass and function requires protein, energy and
clinical implications of these changes are less well nutrient advice.72 The provision of specialist dietary
described, but bone marrow adipocyte accumulation in advice such as pre‐ and probiotics, micronutrients and
both obesity and ageing has been linked to impaired neutropenic diet was rare outside dietitians; this could be
haemopoiesis.57 a result of recognised gaps in nutrition education and
Nutrition guidelines recommend the inclusion of training of non‐dietetic HCPs.73,74 Vitamin D was the
strategies to diagnose and monitor for low muscle most frequently discussed vitamin pre‐HCT, potentially
mass as part of nutritional/dietetic assessments. 17,50 reflecting its emergent role in anaemia,75 infection and
The most appropriate method will depend on GvHD.75,76 thus warranting further HCP training.
resources, staff and training available, alongside the Neutropenic dietary advice was routinely provided;
target population.58 As more research is published, however, the level of restriction advised was not
there is also emerging data on population specific evaluated in this study. While, neutropenic restriction is
reference ranges and adjustment factors to ensure still practiced there is insufficient evidence to support
correct interpretation.58–60 very restrictive practices77 the British Dietetic Associa-
Sarcopenic screening may help identify those at tion has recommended relaxation of restrictions as a
risk of low muscle mass, quickly at scale to support result of gaps in the evidence base.78 Prophylactic tube
early intervention, in time and resource limited feeding was rare with unintentional weight loss and BMI
settings. Although there is a range of available as the primary indicators for feeding, which is in line with
screening approaches for sarcopenia, 61 most were national and international recommendations.19,79
 1365277x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jhn.13315 by Nat Prov Indonesia, Wiley Online Library on [30/06/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
12 | HEALTH PROFESSIONAL ATTITUDES BEFORE HCT

Limitations Snowden contributed to the design, critical review and

revision of the article. JL contributed to distribution of
This survey was comprehensive and allowed greater survey, coordination of some responses from centres and
understanding of interprofessional and between centre article review.
variation than similar studies. However, it was not
possible to obtain representation from all centres or all A C K N OW L E D GE M E N T S
target professionals within a site. There were notable We thank BSBMTCT Clinical Trials Sub Committee for
discrepancies in reported provision of nutritional care facilitating survey dissemination and initial advice on site
between professionals within a site, raising important engagement; Dr Jennifer Byrne, Nottingham University
considerations for other surveys of multiprofessional Hospitals NHS Trust, for identifying BSBMTCT as a
intervention delivery. Increased knowledge of nutrition collaborator; Dr Rachel Pearce, BSBMTCT statistician,
provision within centres and between HCPs could be for initial advice on statistical approaches; Kathryn
improved via inclusion of allied services in multidisci- Blount, Nottingham University Hospitals NHS Trust,
plinary teams, documented processes and nutrition for proof‐reading the manuscript; Dr Sarah Crozier,
training. This study also focused on HCP perceptions Consultant Psychologist, Nottingham University Hospi-
of prehabilitation for HCT as a whole and did not tals NHS Trust and Dr Orla McCourt, Physiotherapist,
explore HCP perceptions on differential service needs by University College London Hospitals for their peer
type of transplant or diagnosis. discussion. There was no allocated funding for this
research.

CONCLUSIONS CONF LICTS O F INTEREST ST ATE MENT

The authors declare that there are no conflicts of interest.
Nutrition and prehabilitation in HCT are perceived as
important and deliverable by HCPs, but current provi- DA TA AV AI LA BI LIT Y S TA TEME NT
sion in UK centres is limited and inconsistent. Although The data that support the findings of this study are
limited, HCT prehabilitation research does exist, future available from the corresponding author upon reason-
studies should include detailed intervention descriptions able request.
in discrete haematological populations, including core
outcome frameworks. Furthermore, although interna- ETHICAL ST ATE MENT
tional HCT18 standards recommend access to allied The study was registered with the Health Research
services, such as dietitians, they lack detail on minimum Authority who confirmed that ethics approval was not
standards of pre, peri‐ and post‐HCT nutrition, relative required. All local governance and GDPR processes were
to the size, throughput and age range of the unit. followed.
Defining minimum nutrition standards in HCT via
national organisations (e.g., BSBMTCT) or refined OR CI D
accreditation standards (Joint Accreditation Committee Laura J. Miller http://orcid.org/0000-0003-3056-5443
ISCT‐Europe & EBMT)18 may help address these unmet
needs, reducing inequalities in access identified in this PEER REVIE W
study, guiding centres and commissioners. Further The peer review history for this article is available at
research is warranted to quantify the impact of nutrition https://www.webofscience.com/api/gateway/wos/peer-
and prehabilitation interventions on survival outcomes, review/10.1111/jhn.13315.
patient experience and health economics associated
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cg32/chapter/Recommendations Additional supporting information can be found online
in the Supporting Information section at the end of this
AUTHOR BIOGRAPHIES article.

Laura J. Miller is a Haematology research dietitian

and NIHR PhD candidate, Nottingham University
How to cite this article: Miller LJ, Halliday V,
Hospitals (NUH) NHS Trust and the School of
Snowden JA, Aithal GP, Lee J, Greenfield DM.
Medicine, University of Nottingham, with extensive
Health professional attitudes and perceptions of
clinical experience in haematological conditions.
prehabilitation and nutrition before
haematopoietic cell transplantation. J Hum Nutr
Vanessa Halliday is a Registered dietitian and faculty
Diet. 2024;1–15. https://doi.org/10.1111/jhn.13315
Director of Education for Health, School of Medicine
and Population Health, University of Sheffield, UK.