The goals of nutrition therapy are to maintain or improve energy and protein intake, mitigate metabolic abnormalities, preserve physical function, reduce the risk of treatment intolerance, and improve quality of life before, during, and after curative or palliative treatment [29]. The nutrition care process is a systematic way of providing nutrition care to patients across healthcare settings and is used to address these goals, which is an important aim of the MDT care approach (Fig. 1) [30].
Not all patients have access to comprehensive nutrition care, in particular when dietitian staffing is insufficient, reimbursement for nutrition services is absent, or screening standards are lacking. In a survey of cancer survivors (n = 1073 responses), fewer than 40% of patients with involuntary weight loss reported being seen by a dietitian during treatment [31]. Trujillo et al. reported that the average dietitian-to-patient ratio in outpatient cancer centers in the USA was 1:2308, far below the estimated ratio of 1:120 needed to provide proactive nutrition care and highlighting the need to expand nutrition resources and improve reimbursement [32].
Many international nutrition societies recognize the importance of nutrition as essential to comprehensive, high-quality oncology care. Societies, including the American Society of Clinical Oncology (ASCO), the American Society of Parenteral and Enteral Nutrition (ASPEN), the European Society for Clinical Nutrition and Metabolism (ESPEN), have published recommendations regarding nutrition care to guide clinical practice and improve patient and healthcare outcomes (Table 1).
Table.1 Nutrition care process – expert organization recommendations Screening for malnutrition risk and low muscle mass
All clinical nutrition societies and several oncology societies recommend screening for malnutrition risk at diagnosis and during and after treatment (Supplementary Table 1). Several validated screening tools are available, such as the Malnutrition Screening Tool (MST), which can be administered quickly by nursing staff [33].
Screening is not mandated in most countries, nor is it standardized. Trujillo et al. reported that 53% of outpatient cancer centers in the USA screened for malnutrition risk and 65% used a validated screening tool [32]. A quality assurance performance improvement program, implemented in outpatient cancer treatment centers to assess the feasibility of standardizing malnutrition screening with a validated tool embedded in the electronic health record/electronic medical record (EHR/EMR), found that the rate of screening increased from 60% at baseline to 78% at 20 months [34].
Because muscle loss is common, the Clinical Oncology Society of Australia recommends all patients be screened for low muscle mass at diagnosis and re-screened when patients’ clinical situations change, using the SARC-F questionnaire alone or in combination with calf circumference (SARC-CalF) [35]. However, these tools have not been fully explored and validated in patients with cancer. SARC-F is a geriatric assessment related to functional outcomes and has not yet been proven to be ideal for use in patients with cancer of all ages, but may have acceptable performance among older patients with cancer [36, 37]. In the aging literature, although SARC-F performs satisfactorily for evaluating muscle function, SARC-CalF has greater screening efficacy than SARC-F for identifying low muscle function and low muscle mass in older adults [38, 39]. Importantly, adjustment factors for the confounding effects of adiposity on calf circumference have been recently published (Table 2) [40]. This study was conducted in a healthy adult population and appears to be the only feasible means to identify low calf circumference in patients with excess weight; its use in clinical practice is yet to be explored [40]. Additional data are needed to fully characterize the screening performance of SARC-CalF in oncology.
Table.2 BMI adjustment factors for calf circumference outside BMI range of 18.5–24.9 kg/m2 by ethnicity/race ( Nutrition assessment to diagnose malnutrition
Nutrition assessment can be conducted using several available tools to evaluate nutrition status, such as the Subjective Global Assessment (SGA) and the Patient-Generated Subjective Global Assessment (PG-SGA) [41, 42]. Nutrition assessment is different from nutrition screening in that it determines the presence, severity, and causes of malnutrition and is used to plan nutrition intervention, while screening indicates the presence or absence of malnutrition risk. [43].
Nutrition societies recommend early nutrition assessment for all at-risk patients before anticancer treatments (including surgery) begin, with reassessments at regular intervals throughout the cancer trajectory (Supplementary Table 2). ESPEN also recommends dual X-ray absorptiometry, anthropometry, bioelectrical impedance analysis, or CT scans to assess muscle mass, and walking tests or dynamometers (i.e., hand-grip strength) for muscle function [29].
With the lack of consensus on the diagnostic criteria for malnutrition, a framework such as the one proposed by the Global Leadership Initiative on Malnutrition (GLIM) can be used to help diagnose malnutrition through (1) identifying at-risk patients using any validated screening tool and (2) conducting a nutrition assessment using validated assessment tools to diagnose and grade the severity of malnutrition. GLIM’s diagnostic criteria include three phenotypic criteria (involuntary weight loss, low BMI, and reduced muscle mass) and two etiologic criteria (reduced food intake or assimilation and inflammation or disease burden) [44].
Interventions
Nutrition therapy is essential in cancer care
Nutrition intervention encompasses nutrition counseling and education, oral nutritional supplements (ONS), and enteral and/or parenteral nutrition support, as appropriate for each individual case. Healthcare providers should proactively identify early indicators of malnutrition risk in their patients (e.g., anorexia and reduced food intake) and intervene with additional protein and energy before cachexia develops, rather than reactively doing so when patients become severely depleted (i.e., refractory cachexia). Intervening early and throughout treatment may help to improve nutrition status and, ultimately, quality and length of life [45]. Nutrition societies recommend intervening early to support an adequate intake during and after treatment that is based on a patient’s total energy and protein needs (Supplementary Table 3 and Fig. 2), disease status, current intake, lifestyle, and food preferences. Several RCTs, systematic reviews, and meta-analyses involving patients with different tumor types and undergoing various anticancer treatments have shown that nutrition therapy improves weight status, energy and protein intakes, treatment tolerance, and survival and reduces nutrition impact symptoms, hospital readmissions, and mortality [12,13,14,15, 46]. While not all evidence supporting oncology nutrition is based on RCTs, the body of evidence is substantial and should not be dismissed. This is an important consideration given the frequency of non-evidence-based medical practice in oncology, which has been reported to occur in 33% of patients [47].
Specific nutrients may have important roles in improving nutrition status while mitigating metabolic changes and the consequential decline in muscle mass and physical function in patients with cancer. One example is eicosapentaenoic acid (EPA), a long-chain omega-3 fatty acid (ω–3) found in fish oil, with some current guidelines recommending EPA or fish oil supplementation to stabilize or improve appetite, and increase food intake, muscle mass, and body weight in patients with cachexia and/or advanced cancer who are undergoing chemotherapy [29, 48]. A systematic review and meta-analysis of 11 RCTs (n = 1350) demonstrated consuming high-protein ONS enriched with ω–3 fatty acids was associated with improved body weight, attenuated lean mass loss, and improved selected domains of quality of life among patients receiving chemotherapy [49].
Exercise is important in cancer care
Aerobic and resistance exercise during anticancer treatments preserves or improves aerobic capacity, muscle mass and strength, and quality of life [50, 51]. Several societies advocate regular exercise before, during, and after treatment as a standard of care in oncology (Supplementary Table 4). Exercise is safe and well-tolerated by most patients with various cancer types [52]. However, patients who have had lung or abdominal surgeries or have ostomies, ataxia, extreme fatigue, severe malnutrition, or bone metastases need to be under the care of physical and occupational therapists, or physical medicine and rehabilitation physicians (in conjunction with the dietitian), and should only undertake the physical activity with their guidance and supervision [52]. Exercise recommendations for most patients with cancer and healthy adults (Fig. 3) are similar, although care must be taken to support the additional energy needs of patients with malnutrition who engage in exercise [53, 54].
Prehabilitation exercise is a structured intervention implemented before surgery, which has been found to be safe, and is often delivered as a combination of moderate, continuous cardiovascular activity in combination with resistance training or high-intensity interval training, with the aim of improving functional capacity and increasing muscle mass pre-surgery or pre-treatment (e.g., within 4 to 6 weeks). Both unimodal (exercise only) and multimodal prehabilitation (exercise with nutrition) programs can facilitate recovery and reduce postoperative complications [55].
Multidisciplinary teams provide multimodal treatment
Multidisciplinary teams are dedicated to developing and providing multimodal, patient-centered care throughout the cancer journey (Fig. 1 and Supplementary Table 5). In a pilot trial (n = 34) integrating a patient-centered, best-practice (i.e., evidence-based) head and neck cancer care model with an MDT approach, malnutrition screening increased from 14 to 88%, and early access to dietitians from 20 to 97%, while unplanned hospital admissions and costs were reduced, and communication and care coordination improved [16]. Of note, oncology nurse navigators, who practice mainly in the USA, can play an important role in the MDT by working closely with patients to ensure improved access to supportive care resources and optimal patient comprehension of the diagnosis and cancer treatment options.
Multimodal therapy is the combination of two or more interventions designed to improve specific outcomes (Supplementary Table 6). Despite the lack of standards to treat cachexia, evidence indicates multimodal therapy including nutrition counseling and ONS to promote protein and energy balance, EPA supplementation and non-steroidal anti-inflammatory drugs to reduce inflammation, and moderate resistance exercise to increase anabolism [56,57,58] will improve outcomes. Current evidence suggests that this type of multimodal intervention is feasible, safe, and associated with improvements in weight and nutrition status, physical performance, and symptom severity and may be beneficial to patients with cachexia and advanced cancers [15, 59]. The Multimodal Intervention Exercise, Nutrition and Inflammatory Medication (MENAC) is an ongoing, international RCT evaluating the effect of an early and sustained multimodal program on changes in body weight, muscle mass, and physical activity in patients newly diagnosed with lung or pancreatic cancer and starting cancer treatment (n = 240) [60].
Another multimodal approach implements a prehabilitation intervention that combines (1) personalized nutrition counseling and supplementation as needed, (2) individualized aerobic and weight resistance exercises, and (3) anxiety reduction and relaxation strategies to prepare patients for the anticipated detrimental effects of surgery. The majority of research has been conducted in surgery patients (94%), with several RCTs showing prehabilitation incorporating these three components facilitated earlier return to pre-surgery physical function levels and was associated with greater gains in muscle mass (compared to rehabilitation), and reduced hospital LOS and healthcare costs [61,62,63,64,65].
Monitoring occurs throughout a patient’s journey
Nutrition monitoring should begin at diagnosis and continue throughout the cancer trajectory. It involves evaluating patients’ response to nutrition and exercise interventions, regularly reassessing nutrition status, and providing follow-up care to support recovery from the detrimental effects of treatment on body composition, physical function, and quality of life (Supplementary Table 7). Along with proactive nutrition and exercise interventions during cancer treatment, continuous monitoring and intervening after treatment can facilitate recovery from anticancer treatments and surgery and improve nutrition status, muscle mass, and physical function. Ensuring the continuity and monitoring of nutrition care is essential, including the transition from hospital to home [66].
Position of the experts on nutrition care for patients with cancer
Recognizing the challenges of caring for patients with cancer, and optimizing patient outcomes with nutrition and exercise interventions, this expert panel recommends combining societies’ recommendations and current evidence to implement the following principles to guide clinical practice (Fig. 4):
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1.
Position oncology nutrition at the center of multidisciplinary care
Ample evidence supports that adequately nourished patients benefit from anticancer treatments and supportive interventions, which lessens the challenges of medical management of this population. One path to positioning oncology nutrition as a standard of care is to ensure that MDT members are educated and trained to screen, evaluate, and monitor at-risk and malnourished patients with cancer and understand how and when to refer to a registered dietitian for more in-depth nutrition care. Most healthcare providers do not receive clinical nutrition education, and it may be low on the list of competing clinical priorities. Some societies, such as ASPEN and ESPEN, provide funding for nutrition fellowships for physicians. Perhaps extending similar educational and training opportunities to nurses would help to elevate the value and importance of oncology nutrition as standard practice within MDTs.
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2.
Partner with colleagues and administrators to integrate a nutrition care process into the multidisciplinary cancer care approach.
In most oncology clinics, nutrition care is usually the domain of dietitians and is managed in isolation. Delivering effective nutrition care is possible when MDT members coordinate and communicate nutrition care (Fig. 1). In addition, patients often receive conflicting information and advice about nutrition from healthcare providers; therefore, all members of the MDT need to be knowledgeable about oncology nutrition so they can provide patients with consistent and accurate nutrition guidance.
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3.
Screen all patients for malnutrition risk at diagnosis and regularly throughout treatment
Nursing-led screening for malnutrition at diagnosis is essential. Organizational processes to standardize screening are recommended, where positive results are documented and communicated to the MDT and patients are referred to a dietitian, as appropriate, for further assessment and follow-up.
Although evidence indicates a high percentage of patients with newly diagnosed cancer have low muscle mass, no validated tools to screen for muscle loss currently exist, representing knowledge gaps researchers and expert societies need to address.
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4.
Combine exercise and nutrition interventions before (e.g., prehabilitation), during, and after treatment as oncology standard of care in oncology to optimize nutrition status and muscle mass
Cancer is a multifaceted disease requiring multimodal interventions best delivered by MDTs. Current guidelines recommend exercise combined with nutrition interventions as a standard of care. Combining these supportive interventions is associated with improving patients’ quality of life and health-related outcomes in cachexia. Perioperative multimodal interventions, such as prehabilitation, can improve physical function, increase muscle mass, and reduce complications among patients undergoing surgery.
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5.
Incorporate patient-centered approaches into multidisciplinary care
In patient-centered, collaborative, and coordinated care, a patient’s health needs and desired health outcomes guide decisions regarding their healthcare. The key components of patient-centered care include patient education and empowerment, patient-centered communication, coordinated and integrated care, and provision of emotional support [67].