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J. Lambert et al.
Prehabilitation: What Does It Mean inHealthcare Contexts?
“Prehabilitation” [1, 2] is a term used to capture interventions to prepare patients for
healthcare treatment, typically surgery. Like a marathon, surgery is a huge stressor
on the human body and training in the form of prehabilitation prepares the body for
this challenge. Prehabilitation interventions typically comprise of exercise, nutrition, and psycho-social support [2] but are multi-factorial and even encompass the
management of tobacco [3], alcohol [4], and other addictions.
Prehabilitation can improve cardiorespiratory tness before cancer surgery [5],
which improves functional capacity and reduces hospital length of stay [2], thus
offering patient-centred and economic benets. Indeed, prehabilitation has the
potential to reduce the peri-operative risk proles of patients who are deemed unt
for major operations. It is generally accepted that reducing complication rates and a
quicker return to baseline functional capacity can accelerate the progression of cancer patients to chemotherapy. Reduced time to chemotherapy has been seen in some
cancer cohorts to offer a survival benet [6]. We have yet to identify a prehabilitation strategy that works for everyone; and like many exercise interventions [7], there
is a heterogenous response to prehabilitation.
What Should Prehabilitation Comprise of?
Exercise
Programmes are designed to improve cardiovascular tness and physiological
reserve, to build muscle and improve strength, and augment well-being and psychological resilience. Most exercise programmes comprise of a combination of aerobic
and strength training, delivered via a supervised or unsupervised format. This may
involve a graded regime where patients complete a form of aerobic training at a
percentage of their maximal heart rate, and increase this percentage every week to
achieve a specied level of exertion (mild, moderate, or high intensity).
Published data suggests that bespoke supervised exercise interventions outperform unsupervised formats in achieving exertional intensity and compliance.
Breathing exercises have also been suggested as a useful way of improving the
function of the muscles of breathing and as a stress-reduction strategy [8].
Patients diagnosed with gastrointestinal (GI) malignancies often present with a
series of clinical signs including tiredness, weight loss, anaemia, and jaundice.
These signs often coincide with long periods of under-nutrition and deconditioning.
The highest frequency of GI malignancy presentation is within the sixth to eighth
decades, where sarcopenia may be another compounding factor. Several recent
studies have alluded to poor muscle quality and function as an independent predictor of adjuvant chemotherapy toxicity, morbidity, and mortality in GI cancer surgery
[9, 10].
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Diminished Oxidative Stress
There is evidence to suggest that exercise may modulate the tumour microenvironment by reducing pro-inammatory mediators associated with tumour
spread [11]. Exercise may play an anti-inammatory role by reducing oxidative
stress [12], which may be important in patients undergoing concurrent chemotherapy and radiotherapy treatment. Although the psychological aspects of exercise
within prehabilitation have not been extensively studied, there is evidence to suggest that exercise may improve psychological resilience peri-operatively [13]. This
could be paramount in patients living with indolent or recurrent disease.
Within the clinical context, cardiopulmonary exercise testing (CPET), peak expiratory ow rates, and hand grip strength may be used to objectively measure
improvements in tness. However, outside clinical trials, these measures are rarely
used for this purpose due to cancer target times, resourcing, and scheduling constraints. The challenge in designing exercise regimes revolves around a protocol that
is acceptable in terms of ease of completion and scalability, while also being effective with high compliance and adherence.
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Nutrition
The main goal of nutrition in prehabilitation is to rst ensure that patients are eucaloric, then aiming to supplement macronutrients and micronutrients guided by a
dietician within a multi-disciplinary team (MDT). This process often involves
screening using the Malnutrition Universal Screening Tool (MUST), which is common in the UK settings but also used worldwide and based on the most recent
European Society of Clinical Nutrition and Metabolism (ESPEN) guidelines . In
addition, in patients with malignant biliary obstruction, pancreatic enzyme replacement therapy was associated with improved survival [14]. Within clinical practice,
it would be benecial to supplement patients as early as possible within their treatment pathways, and even prior to enrolment on a formal prehabilitation programme.
Although there is no specic nutrition regime that guarantees caloric goal
achievement, carbohydrate, protein, fat, and micronutrient supplementation are
commonplace. In GI cancer patients, there is often weight loss directly because of
mechanical obstruction and/or malabsorption, and indirectly through tumour wasting effects or cachexia, often mediated through cytokine signalling pathways [15].
Commercial Supplements
Several regimes including whey protein [16, 17], fortied protein drinks [18], and
amino acid-based compounds [19] have been used in controlled trial settings and
more liberally based on hospital protocols. As a standalone measure, the impact of
nutrition on outcomes has been difcult to quantify due to the integrated biological
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and physiological pathways through which nutrition may exert its effects. Details
from prehabilitation trials involving supplementation suggest that timing of ingestion; usually just prior to or after exercise may be more benecial as this relates to
metabolism of substrates, especially regimes focused on building muscle.
The effect of nutrition may be best appreciated when employed within a
multi- modal programme due to its synergy with exercise. Various delivery
methods such as nasogastric, nasojejunal, and gastrostomy routes may be used
in cases where there may be some anatomical anomaly, other gut dysfunction,
or where feeding needs to be accelerated. Parenteral feeding is now indicated
only in exceptional circumstances given its high costs, substantial morbidity,
and inferior benets.
J. Lambert et al.
Psycho-Social Support
Talking therapies and formal counselling, when integrated into multi-modal prehabilitation programmes, are associated with reduced levels of treatment related stress
[20, 21]. As previously mentioned, there appears to be a positive association between
exercise and improved well-being/psychological resilience. What is clear from
other data concerning psychological challenges in cancer diagnoses in general, is
that there may be several interrelated factors (biological, personal, and social) in the
way patients perceive and manage illness [22]. Meaningful relationships, family
support, baseline health, prior illnesses, and cancer diagnoses all contribute to the
way patients may choose to deal with their illness, and their levels of engagement
with cancer care teams.
Cessation ofSmoking andAlcohol
It is now universal practice to support patients with nicotine and alcohol dependence
by offering advice and interventions to facilitate cessation. These may take the form
of pharmacological treatments such as nicotine replacement or psychosocial therapies. Smoking cessation may improve patients exercise tolerance and when considered within a prehabilitation exercise programme is likely to improve adherence.
Likewise, alcohol dependence is often associated with macronutrient and micronutrient deciencies that may impact on substrate utilisation and impede the positive
adaptive effects following exercise.
While these interventions are likely to work alongside prehabilitation programmes, they are also important public health interventions that have long
been established in the promotion of healthier lifestyles. The evidence suggests
that smoking cessation for even relatively short durations preoperatively
(2 weeks) [23] can reduce morbidity and complications in the peri-operative period.
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Obesity Reduction
While prehabilitation may provide a platform for patients to adopt more healthy
lifestyles postoperatively, in clinical practice, it is often unrealistic to expect considerable weight reduction within cancer operative timescales. For this reason, the success of prehabilitation programmes will inevitably depend on a community-based
approach in promoting healthier lifestyles as part of a wider cancer risk reduction
strategy.
Management ofOther Medical Conditions
andPharmacological Treatments
Other important factors centred around peri-operative care include management of
preoperative anaemia, blood glucose, rationalisation of medications, and optimising
the treatment of any underlying chronic cardiorespiratory conditions such as atrial
brillation, heart failure, and chronic obstructive pulmonary disease (COPD).
Within healthcare systems, entire departments have evolved to adopt this important
aspect of peri-operative optimisation. They are often given names such as ‘Surgery
School’ to focus patients minds as to what they are likely to encounter when referred.
In addition to giving procedure specic information, patients are also signposted to
resources and support groups, and are given key-worker contact details. This aspect
of care is often delivered by a multi-disciplinary team (MDT).
How Long Should Prehabilitation Be?
One of the greatest challenges of prehabilitation is the limited time available to
intervene, particularly in circumstances of cancer. Unlike rehabilitation or enhanced
recovery after surgery (ERAS) [24] where there are no time pressures, the National
Health Service (NHS) in the UK and other world-healthcare bodies have timelines
to start treatment, to maximise treatment outcomes. Indeed, prehabilitation should,
where possible, not interfere with these timelines and rarely exceeds 31days from
a decision to treat. This timescale suggests that ideally one should start prehabilitation even before the point of diagnosis.
To manipulate changes in physiological function such as muscle metabolism or
cardiorespiratory tness, the minimum period to exert viable improvements is likely
2–4weeks [21, 25]. Smoking and alcohol cessation are likely to complement and
enhance the effectiveness of other strategies such as exercise and nutrition. Targets
of cardiovascular tness such as anaerobic threshold and peak oxygen consumption
can be achieved on a 6-week high intensity exercise programme [26]. In turn, weight
reduction in obese patients is likely to take much longer.
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J. Lambert et al.
Cancer 4–6Week Protocols
These are average routines, within a wider range. Patients undergoing long-course
chemoradiotherapy for advanced rectal cancer have much longer times to participate in prehabilitation programmes, in some cases up to 9weeks [27]. Within clinical trial environments, high motivation may inuence the likelihood of completing
prehabilitation regimes. In real life, chemo or radiotherapy side-effects preclude
participation or completion of programmes, besides time constraints with cancer
targets, personal patient factors, and surgery dates. Rather than offer a generic programme for a large cross-section of patients, resources may have to be targeted to
the most ‘at risk’ groups, customised to their needs.
What Protocols are Typically Employed forPrehabilitation?
One author is currently involved in an NIHR study to map prehabilitation services
across the UK (NIHR134282). Data collected to date show a wide spectrum of practice
ranging from hospitals delivering no formal prehabilitation programmes to established,
research-informed, multi-modal prehabilitation offers to most cancer patients. Those
that offer prehabilitation programmes often fall into two groups (preoperative interventions versus pre- and postoperative interventions). In general, for gastrointestinal cancer
surgery, the total time available before surgery is rarely over 9–12weeks, with most
being 4–6weeks; this period is often dictated by the type of cancer and whether neoadjuvant therapy is required prior to surgery. Other factors such as correction of anaemia,
biliary drainage, and pharmacological optimisation of chronic conditions may also
extend the time before surgery and offer a longer window for prehabilitation.
Who Should Deliver Prehabilitation?
The world’s population is ageing such that by 2050, the number of over-60s will
nearly double from 12% to 22% [28]. This will further stress healthcare systems
across the globe and indeed, in the UK, waiting lists for elective surgery are currently the longest on record with 7.3 million people [29].
Prehabilitation is essential to optimise patient outcomes, but nonetheless, represents an additional burden on top of already stretched healthcare providers such as the
NHS.Many prehabilitation programmes are delivered as part of the multi- disciplinary
team (MDT) managing a patient’s overall cancer care. The exercise interventions
themselves can be delivered by local council gyms, private health clubs, and even
football clubs in a local community, harnessing the power of existing infrastructure
[30]. Nutrition advice can be delivered in these environments and also inlocal com-
munity settings such as you have for weight-loss clubs or similar.
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Prehabilitation Clinics
These could be delivered by the private sector. They would need to include cardiopulmonary exercise testing (CPET), dietary analysis, and provision of dietary
advice, and access to councillors or clinical psychologists, to ensure the psychological welfare of those undergoing prehabilitation. There is also the potential to
empower patients to undertake prehabilitation themselves, seeking advice from
both within and external to the MDT, perhaps including community support groups.
This approach does, however, have potential risks. Cancer patients are clinically
vulnerable and it’s important that any intervention whether inpatient, outpatient or
in the community is research informed, and those delivering any service are appropriately trained and resourced to deal with adverse events that are more likely in this
than the general population.
How Could WeFacilitate Remote Prehabilitation?
Remote prehabilitation removes any space or human resource requirement from
healthcare providers, and it is scalable across a population at limited cost. However,
adherence rates fall from >95% in hospital-based (supervised) prehabilitation interventions to 70% in remote unsupervised prehabilitation [31]. Compliance is a major
determinant of the success, and the protocol should be similarly tailored to the
patient’s aerobic tness, lifestyle, and personal preferences where appropriate [32].
It is also critical that some level of supervision is maintained throughout any intervention, to maximise adherence [32].
We can learn a lot from the space industry where exercise and nutrition interventions, and medical care, have been delivered remotely since 1971, onboard a space
station, the Soviet Union’s Salyut [33]. Two basic principles from spaceight missions and telemedicine can be adopted for remote Prehabilitation: gastrointestinal
cancer surgery: (1) health screening and (2) remote monitoring and
communication.
Principles ofTelehealth
High-risk participants may not be suitable for a remote intervention where medical
help may not immediately be at hand. These might include cases with frailty who
are at high risk of falls [34] but also cardiovascular abnormalities such as atrial
brillation, where exercise might pose a threat of a signicant adverse event, or
those with a V O
≤18mL/min/kg [35]. Remote supervision can also be highly relevant. Depending
on the patient and the intervention, this may need to be real-time monitoring of heart
peak (highest amount of oxygen consumed during exercise)
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rate or ECG.It could encompass the delivery of exercise interventions over webbased video platforms, or online consultations with psychotherapists. A key tenet of
remote interventions is that participants do not feel they are left to do things completely independently, as we know this negatively affects compliance with interventions and ultimately leads to high attrition rates [36].
The advent of new healthcare technologies (wearable devices) could be used to
monitor the health of participants whilst exercising and advise the participant to
adjust their effort accordingly.
J. Lambert et al.
How Can WeHarness New Technologies toFacilitate
Remote Prehabilitation?
The window between diagnosis and surgical treatment presents a unique opportunity where patients are more engaged and motivated for positive behaviour change,
to maximise their health outcomes [37]. However, large scale implementation of
prehabilitation is challenging due to the gap that currently exists between the
resources and demands of healthcare services [38]. The use of digital technologies,
so-called telehealth or telemedicine forms part of a solution to this problem, to
deliver prehabilitation in a sustainable and efcient way [39]. Engagement in a
patient’s own treatment has been shown to improve patient outcomes [40] and
home-based prehabilitation can be used to empower patients to play an active role
in their treatment pre-surgery.
One of our own prehabilitation studies (SPECS, NCT04880772) employed a
remote prehabilitation intervention as the study was started during the pandemic.
The delivery of the exercise prehabilitation classes remotely over a web-based platform removed the need for patients (typically clinically vulnerable) to enter an environment with known coronavirus infections during the pandemic, thus reducing the
risk of the prehabilitation offer. COVID-19 has accelerated the uptake of technologybased interventions and revolutionised patient care, certainly in primary care where
30% of appointments currently take place remotely, accounting for some 7.4 million appointments in the UK every year [41].
Limitations toWidespread Adoption ofPrehabilitation
Such include patient access in remote areas, those of low socio-economic status
who perhaps cannot afford frequent transport costs to and from a rehabilitation centre, and the nite time available with challenges of work, family-life, and other
medical appointments in the run up towards surgery [42]. Technology-based prehabilitation can circumvent these limitations, thus increasing accessibility to prehabilitation and potentially reducing health inequalities.
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Technologies can be app-based; web-based; video or game digital-based technology; and virtual reality [42]. Smart watches and mobile phone apps can be used
both in the delivery of a prehabilitation intervention and in monitoring uptake and
adherence of any intervention [43]. Evidence from a recent pilot study suggests that
commercially available smart watches and associated apps can increase the volume
of moderate and vigorous physical activity that patients undertake, and this results
in an increase in functional capacity when measured by the 6-min walk test [43].
A major challenge to the implementation of any technology-based prehabilitation is the paucity of high-quality research on their efcacy. In a recent review of 11
RCTs, none measured complication rates, length of hospital stays, or readmission
rates [39]. The psychosocial improvements of telehealth interventions appear the
most well-documented, with increased return to work, reduction in pain catastrophising, and an improved perception of preparedness for surgery [39].
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Should All Gastrointestinal Cancer Patients BeEnrolled?
From a biological disease point of view, we have not found any factors that preclude
participation in prehabilitation, for any modality of gastrointestinal cancer. Time to
cancer diagnosis and survivability have been viewed as quality measures of how
well or poorly healthcare systems are functioning including the NHS (NHS England
and NHS Improvement 2022). The concept of fast-track surgery is now commonplace in some units with highly selective patient criteria. This may present a challenge for prehabilitation services due to obvious time constraints.
Within the context of nancial pressures the highest risk patients should be prioritized, in whom prehabilitation is likely to benet the most. Strategically used
available resources may seamlessly yield results provided that primary, secondary,
social care systems can be integrated through better arrangements, data management, and use of healthcare technology. A useful starting point could be simply a
reorganisation of patient treatment pathways where high-risk groups could be identied at primary care levels and referred to a prehabilitation service as a matter of
course, like the way patients are referred as 2-week wait referrals for a new cancer
diagnosis.
What are theOutcomes ofPrehabilitation?
We have shown that there is a signicant but modest reduction of length stay by
1.8days in hepatobiliary, colorectal, and upper gastrointestinal cancer surgery [2].
Larger cohorts and longer follow ups may be needed. If morbidity and mortality are
no different within a year of surgery, does this truly mean there is no effect
longer-term?
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J. Lambert et al.
Prehabilitation programmes are effective at improving exercise capacity both
before and after gastrointestinal cancer surgery. A meta-analysis demonstrated that
6-min walking distance was improved by 33m before surgery and 48m 4–8weeks
after surgery [44]. However, no difference in Clavien-Dindo ≥ III complication
rates was found. Additional studies have reported no effect on postoperative complications, hospital readmissions, mortality, and even hospital length of stay [45],
though this latter result contrasts with our own [2].
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