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DOI: 10.1002/jpen.2420

REVIEW‐SYMPOSIUM

Nascent to novel methods to evaluate malnutrition and frailty

in the surgical patient

Carla M. Prado PhD, RD1 | Katherine L. Ford MSc, RD1 |

2
M. Cristina Gonzalez MD, PhD | Lisa C. Murnane MND, APD3,4 |
Chelsia Gillis PhD, RD5 | Paul E. Wischmeyer MD6 | Chet A. Morrison MD7 |
8,9
Dileep N. Lobo DM
1
Department of Agricultural, Food & Nutritional Science, University of Alberta, Edmonton, Alberta, Canada
2
Postgraduate Program in Health and Behavior, Catholic University of Pelotas, Pelotas, Brazil
3
School of Allied Health, Human Services and Sport, La Trobe University, Melbourne, Victoria, Australia
4
Department of Nutrition and Dietetics, Alfred Health, Melbourne, Victoria, Australia
5
School of Human Nutrition, McGill University, Montreal, Quebec, Canada
6
Departments of Anesthesiology and Surgery, Duke University School of Medicine, Durham, North Carolina, USA
7
Department of Surgery, Central Michigan University, Saginaw, Michigan, USA
8
Gastrointestinal Surgery, Nottingham Digestive Diseases Centre and National Institute for Health Research (NIHR) Nottingham Biomedical Research Centre,
Nottingham University Hospitals NHS Trust and University of Nottingham, Queen's Medical Centre, Nottingham, UK
9
MRC Versus Arthritis Centre for Musculoskeletal Ageing Research, School of Life Sciences, University of Nottingham, Queen's Medical Centre, Nottingham, UK

Correspondence
Carla M. Prado, PhD, RD, Department of Abstract
Agricultural, Food & Nutritional Science,
Preoperative nutrition status is an important determinant of surgical outcomes, yet
University of Alberta, 8602 112th Street NW,
Edmonton, AB T6G 2E1, Canada. malnutrition assessment is not integrated into all surgical pathways. Given its
Email: [email protected]
importance and the high prevalence of malnutrition in patients undergoing surgical
Funding information procedures, preoperative nutrition screening, assessment, and intervention are
National Institutes of Health, needed to improve postoperative outcomes. This narrative review discusses novel
Grant/Award Number: NIH R01HD107103
methods to assess malnutrition and frailty in the surgical patient. The Global
Leadership Initiative for Malnutrition (GLIM) criteria are increasingly used in surgical
settings although further spread and implementation are strongly encouraged to
help standardize the diagnosis of malnutrition. The use of body composition
(ie, reduced muscle mass) as a phenotypic criterion in GLIM may lead to a greater
number of patients identified as having malnutrition, which may otherwise be
undetected if screened by other diagnostic tools. Skeletal muscle loss is a defining
criterion of malnutrition and frailty. Novel direct and indirect approaches to assess
muscle mass in clinical settings may facilitate the identification of patients with or at
risk for malnutrition. Selected imaging techniques have the additional advantage of
identifying myosteatosis (an independent predictor of morbidity and mortality for
surgical patients). Feasible pathways for screening and assessing frailty exist and

This is an open access article under the terms of the Creative Commons Attribution‐NonCommercial License, which permits use, distribution and reproduction in any
medium, provided the original work is properly cited and is not used for commercial purposes.
© 2022 The Authors. Journal of Parenteral and Enteral Nutrition published by Wiley Periodicals LLC on behalf of American Society for Parenteral and Enteral Nutrition.

S54 | wileyonlinelibrary.com/journal/jpen J Parenter Enteral Nutr. 2023;47:S54–S68.

 19412444, 2023, S1, Downloaded from https://aspenjournals.onlinelibrary.wiley.com/doi/10.1002/jpen.2420 by Cochrane Colombia, Wiley Online Library on [16/02/2023]. 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
JOURNAL OF PARENTERAL AND ENTERAL NUTRITION | S55

may determine the cost/benefit of surgery, long‐term independence and productiv-

ity, and the value of undertaking targeted interventions. Finally, the evaluation of
nutrition risk and status is essential to predict and mitigate surgical outcomes.
Nascent to novel approaches are the future of objectively identifying patients at
perioperative nutrition risk and guiding therapy toward optimal perioperative
standards of care.

KEYWORDS
body composition, frailty, GLIM, imaging, malnutrition, muscle mass, nutritional assessment,
nutritional risk, nutritional screening, perioperative nutrition, sarcopenia, surgery

Preoperative nutrition status can be optimized and is a modifiable risk induced by preoperative nutrition risk or malnutrition extends
factor for surgical outcomes.1 The impact of malnutrition on adverse hospital length of stay and incurs added financial cost.12 Poor
surgical outcomes has been repeatedly demonstrated, yet screening nutrition status can adversely affect humoral and cell‐mediated
for the presence or risk of malnutrition in this context is not immune responses, which, in turn, impair normal functioning of
integrated into all surgical pathways.2 Furthermore, few at‐risk neutrophils and the ability of inflammatory cells to respond to
patients receive nutrition therapy preoperatively.2,3 Given that up infection.8 The humoral agents further promote proinflammatory
to 65% of patients admitted to the hospital for surgical procedures cytokine generation from the surgical site, which stimulates whole‐
present with malnutrition or are at nutrition risk, preoperative body protein catabolism via glycolysis and proteolysis.13 These
nutrition screening and intervention are needed to improve post- immune processes are sensitive to changes in nutrition status, and
operative outcomes.2,4–7 This narrative review focuses on nascent to even a short period of protein‐energy malnutrition induces negative
novel methods to evaluate nutrition risk, status, and frailty in the immunological changes in the surgical patient in a prolonged fasting
surgical patient. or malnourished state.8
The need for optimal nutrition extends beyond the preoperative
period and is a critical component of the perioperative care
I M P O R T A N C E O F N U T R I T I O N S T A T U S ON continuum.14 Widespread integration of Enhanced Recovery After
SURGICAL OUTCOMES Surgery (ERAS) guidelines has increased awareness of the importance
of preoperative nutrition optimization and has reduced the perio-
Preoperative nutrition status influences a patient's ability to tolerate perative fasting time for the surgical patient through introduction of
surgical stress, rate of wound healing, postoperative physical oral carbohydrate loading before surgery and early feeding after
recovery, length of hospital stay, risk of infection, risk of anemia, surgery in addition to other interventions to improve recovery.15,16
gastrointestinal transit time, skeletal muscle health, and overall risk These measures have improved postoperative outcomes,17 but
8–11
of postoperative complications (Figure 1). Delayed recovery widespread dissemination and adoption of ERAS protocols and other

F I G U R E 1 Graphic illustration of the

effect of preoperative nutrition status on
surgical outcomes. Please see supplementary
material for an alternative version of the figure
with North American spelling.
 19412444, 2023, S1, Downloaded from https://aspenjournals.onlinelibrary.wiley.com/doi/10.1002/jpen.2420 by Cochrane Colombia, Wiley Online Library on [16/02/2023]. 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
S56 | PRADO ET AL.

nutrition‐focused protocols are needed to improve surgical amino acid reserves.22,23 Notably, a patient's preoperative nutrition
outcomes, especially the preservation of muscle mass. status determines how acutely critical the catabolic response is
(Figure 2).24 The inflammatory response to surgery and absence of
protein and energy intake (common with traditional care) foster the
S UR G I C A L STR ES S P R O V O K E S perfect storm for muscle breakdown/loss. This is particularly
CATABOLIS M, WHICH INFL UENCES problematic for older adults and those with preexisting malnutrition
POSTOPERATIV E RECOVERY or low muscle mass.
Low muscle mass is a diagnostic criterion for malnutrition.25 Thus,
Preoperative nutrition status is especially important, as it represents these conditions are often observed concurrently and share several
the patient's baseline health status before the trauma introduced by consequences, including postoperative complications, the need for
1
surgical stress. The homeostatic state responsible for maintaining rehabilitation, increased time to wound healing, greater length of
body composition is disrupted by the metabolic response to surgery, hospital stay, falls and fractures, physical impairment, oncologic
which causes breakdown of fat and glycogen stores.13,18 Contrary to treatment toxicity, shorter survival, and poorer quality of life.26,27
starvation in the absence of inflammation, in which body fat is The negative impacts incurred from low muscle mass and/or
mobilized in response to prolonged negative energy balance, surgery malnutrition can all lead to further health consequences, many of
induces an inflammatory response that instigates catabolism.13 In a which also promote additional muscle loss and impact functional
catabolic state, skeletal muscle is broken down and hepatic uptake of recovery postoperatively. The interplay between malnutrition, sarco-
amino acids supports gluconeogenesis and synthesis of acute‐phase penia (low muscle mass and function), frailty, and cachexia is a
proteins.13,19 The metabolic response in combination with the continuum of progressive physiological decline28 that surgical patients,
previously mentioned immunologic changes observed in the surgical especially older adults, are at risk of. Therefore, early and continued
patient results in loss of fat‐free mass, including skeletal muscle nutrition assessment and intervention are needed to avoid negative
mass.13 Furthermore, major surgery has also been shown to outcomes, including the rapid loss of muscle, in the perioperative
adversely affect muscle mitochondrial function, which can lead to period, which can be compared with a wildfire—preventing or
muscle atrophy.20 ameliorating nutrition decline is better than reversing it.29
Skeletal muscle is a metabolic organ that accounts for approxi-
mately 40% of body mass and serves several functions, including
housing the body's largest amino acid reserve, synthesizing and A S S E S S I N G MA L N U T R I T I O N : A F O C U S O N
storing glutamine, regulating blood glucose concentrations, and NOV E L AN D N A S C E NT ME TH O D S
producing myokines.21 More commonly, skeletal muscle is recognized
for its structural functions, including movement, balance, posture, The first step in assessing malnutrition is nutrition screening. As
and bodily strength. In a homeostatic state, muscle mass is tightly summarized elsewhere30 and in Figure 3, screening for nutrition risk
regulated through muscle protein turnover, but in times of starvation can be done using quick and simple methods to assess those at
or inadequate protein intake, muscle protein synthesis is down- immediate risk for malnutrition. Any frontline personnel can perform
regulated and autophagy pathways upregulated to self‐sacrifice nutrition screening.31,32 Nutrition assessment, however, is a more

F I G U R E 2 Graphic representation depicting how a patient's preoperative nutrition status determines how critical the catabolic response is.
The catabolic stress response is associated with muscle loss (and likely weight loss). However, patients who already have low muscle mass are at
greater risk of depleting already compromised reserves, which increases the risk of unfavorable outcomes. Computerized tomography images
were used as an example of a method to evaluate changes in body composition (third lumbar vertebra, patients with normal body weight before
surgery).
 19412444, 2023, S1, Downloaded from https://aspenjournals.onlinelibrary.wiley.com/doi/10.1002/jpen.2420 by Cochrane Colombia, Wiley Online Library on [16/02/2023]. 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
JOURNAL OF PARENTERAL AND ENTERAL NUTRITION | S57

complex and resource‐intensive process, requiring a dietitian/nutri- A summary of commonly used nutrition screening and assess-
tion professional to conduct a detailed evaluation of nutrition status ment tools to evaluate malnutrition in surgical settings is available
(Figure 4). This step allows for a comprehensive assessment, which elsewhere.31 Screening/assessment efforts should start at the
will inform the remainder of the nutrition care process (ie, diagnosis, community level with primary care physicians and healthcare
intervention, monitoring, and evaluation). Nutrition assessment can professionals, as preexisting malnutrition and frailty are related to
be done using a variety of approaches, such as anthropometric and its prevalence in the community. As much as possible, these
body composition measurements; food and nutrition‐related history; conditions should be identified and treated before patients need to
clinical signs; biochemical data; medical tests, procedures, and be admitted to the hospital.
diagnosis; and functional assessment. With regard to novel/nascent methods, a targeted perioperative
nutrition screening tool, the Perioperative Nutrition Score, has been
developed via an international guideline process for perioperative
nutrition screening and has demonstrated predictive validity.2,33 This
score was devised to be simple to incorporate into the electronic
medical record and can be used to rapidly screen for perioperative
malnutrition risk. Nonetheless, further studies are needed to compare
its performance against validated tools.
In view of the COVID‐19 pandemic, a simple remote nutrition
screening tool called the R‐MAPP (Remote – Malnutrition APP) has
been made available for primary care practice.34 The tool involves the
use of the Malnutrition Universal Screening Tool (“MUST”) and
SARC‐F (five‐item questionnaire: strength, assistance with walking,
rise from a chair, climb stairs, and falls), which are simple and
F I G U R E 3 Summary of selected differences between nutrition validated clinical tools to identify nutrition and sarcopenia risk
screening vs assessment. Nutrition assessment can be done using a (SARC‐F being appropriate for older adults).
variety of approaches, such as anthropometric and body composition
Another relatively recent advance in diagnosing malnutrition is
measurements, food‐ and nutrition‐related history, clinical signs,
biochemical data, medical tests, procedures and diagnosis, and functional the development of the Global Leadership Initiative for Malnutrition
assessment. Please see supplementary material for an alternative version (GLIM) criteria.35,36 In a two‐step approach, nutrition risk is
of the figure with North American spelling. evaluated, followed by diagnosis, which includes classifying the

F I G U R E 4 Overview of Global Leadership Initiative on Malnutrition (GLIM) criteria. GLIM is an effort to adopt a global consensus on criteria
for malnutrition diagnosis. It does not exclude the use of other nutrition assessment tools to guide individualized care and treatment. As such,
GLIM is to be used alongside nutrition screening and assessment. Phenotypic and etiologic criteria were derived from commonly used nutrition
screening and assessment tools. Malnutrition diagnosis is based on the identification of one phenotypic and one etiologic criterion. When
present, severity of malnutrition is then determined.35,36 BMI, body mass index; CNST, Canadian Nutrition Screening Tool; MNA, Mini
Nutritional Assessment; MNA‐SF, Mini Nutritional Assessment—Short‐Form; MST, Malnutrition Screening Tool; MUST, Malnutrition Universal
Screening Tool; NRS‐2002, Nutritional Risk Screening‐2002; PG‐SGA, Patient‐Generated Subjective Global Assessment; SGA, Subjective Global
Assessment. Please see supplementary material for an alternative version of the figure with North American spelling.
 19412444, 2023, S1, Downloaded from https://aspenjournals.onlinelibrary.wiley.com/doi/10.1002/jpen.2420 by Cochrane Colombia, Wiley Online Library on [16/02/2023]. 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
S58 | PRADO ET AL.

severity of malnutrition (Figure 4).35,36 A lack of coordinated promotes the use of this approach.43,44 This publication provides
malnutrition assessment and reporting has made clinically relevant consensus‐based guidance on the assessment of skeletal muscle
comparisons between trials and the pooling of results for meta‐ mass using a variety of tools and techniques.43,44
analyses difficult. As such, use of the GLIM criteria in surgical settings
is strongly encouraged to help standardize the diagnosis of
malnutrition in clinical practice, as well as the possibility of Laboratory markers
systematically evaluating malnutrition research worldwide. Notably,
GLIM can be applied by any healthcare professional. In settings A position paper from the American Society for Parenteral and Enteral
where a screening/assessment of malnutrition is already collected, Nutrition (ASPEN) provided guidance on the use of visceral proteins as
information from these tools can be used to conduct the GLIM nutrition markers.45 Serum albumin has been historically considered a
assessment (eg, Subjective Global Assessment, Patient‐Generated marker of surgical risk. However, the authors highlighted that serum
Subjective Global Assessment, Mini Nutritional Assessment) albumin and prealbumin (transthyretin) concentrations are not compo-
(Figure 4). As such, and importantly, GLIM criteria are an additional nents of updated malnutrition definitions, nor should they be used as a
approach to be used alongside nutrition screening and assessment proxy to measure total body protein or muscle mass.45 Although serum
tools and are not meant to replace these steps. albumin and prealbumin are not nutrition markers, their assessment
could be useful as prognostic markers.
A recent study in medical inpatients at nutrition risk suggested
The GLIM criteria that low concentrations of serum albumin at admission had
prognostic implications and indicated higher mortality risk. However,
The use of the GLIM criteria has increased exponentially since this marker was not helpful in selecting patients for nutrition
publication,37 including in surgical settings.38–42 Fiorindi et al.41 interventions, nor did a change in serum albumin concentration
applied the GLIM criteria in a pilot study of patients with predict a response to nutrition therapy.46 As such, whether serum
inflammatory bowel disease undergoing surgery; patients were albumin and prealbumin concentrations can be used to monitor the
evaluated as having Crohn's disease or ulcerative colitis. Forty‐two delivery and efficacy of nutrition intervention is unclear, as serum
percent were malnourished according to GLIM, which was higher albumin concentration may only improve when other inflammatory
than the prevalence identified by the other tools.41 Previous surgery markers are stable.45 Improved serum albumin concentrations in a
for inflammatory bowel disease, disease recurrence, and presence of patient's clinical evaluation may indicate a number of possible
ileostomy were factors that most predisposed patients to mal- scenarios such as improved nutrition status (reduced nutrition risk),
nutrition. Kakavas et al.38 explored the ability of the GLIM criteria to reduced inflammation, correction of fluid shifts, transition to
predict postoperative pulmonary complications after abdominal anabolism, and changes in energy and protein needs.45 However, in
surgery in patients with cancer. In this study, 70% of patients were the short‐term, serum concentrations are more affected by inflam-
identified as malnourished. The risk for postoperative pulmonary mation and fluid balance than by malnutrition or nutrition repletion.
complications was almost two times higher in malnourished patients
than in well‐nourished patients (relative risk [RR] = 1.82; 95%
confidence interval [CI], 1.21−2.73); likewise, the risk for 90‐day Muscle mass
all‐cause mortality was almost twice as high in those classified as
severely malnourished (RR = 1.97; 95% CI, 1.28−2.63). As mentioned earlier, low muscle mass is prevalent in and significant
The GLIM criteria were applied by Boslooper‐Meulenbelt et al.39 to the surgical patient. Several tools can be used to assess muscle
in renal transplant recipients; 14% were malnourished in spite of mass or its related compartments (fat‐free mass, lean soft tissue,
being stable outpatients. Of these, 91% met the phenotypic criterion terminology fully discussed elsewhere47) (Figure 5). Body composi-
of reduced muscle mass within the GLIM framework. Using the GLIM tion assessment is fundamental for the identification of hidden
criteria, Emsley et al.40 showed that 59% of patients who received a muscle abnormalities (Figure 6) and, hence, nutrition status. Low
lung transplant presented with malnutrition. Similarly, Boslooper‐ muscle mass can occur in spite of adequate, excessive, or stable body
Meulenbelt et al.39 showed that a greater proportion of patients were weight (ie, weight stability may mask unfavorable shifts in body
diagnosed as malnourished because of the phenotypic GLIM criterion composition).31,48,49
of reduced muscle mass (47% of all patients), compared with other When body composition assessment is not available, anthro-
approaches used in the study to define malnutrition. pometry can be used as a surrogate tool. The most recent
Collectively, these findings suggest that GLIM criteria are less advancement in the field relates to the measurement of calf
conservative, identifying a greater number of patients with mal- circumference. Calf circumference is widely used as a marker of
nutrition. This may be explained by the use of body composition (ie, muscle mass in clinical practice, as it is highly correlated with skeletal
reduced muscle mass) as a phenotypic criterion in GLIM, as this could muscle mass, especially in the context of sarcopenia assessment in
be undetected by other diagnostic tools. The GLIM guidance for the older adult50; it is a simple, accessible, and low‐cost approach.
the assessment of the muscle mass phenotypic criterion further Whereas this measurement by itself is not novel, recently published
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JOURNAL OF PARENTERAL AND ENTERAL NUTRITION | S59

F I G U R E 5 Summary of pros and cons of

commonly used anthropometric and body
composition approaches to estimate/measure
muscle mass. BMI, body mass index.

F I G U R E 6 Graphic representation
depicting hidden abnormalities in body
composition. Low muscle mass may be hidden
in individuals with normal body weight and
those living with larger body sizes.
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S60 | PRADO ET AL.

adjustment factors allow for the elimination of the confounding than half (56%) of patients had myosteatosis, and this was associated
effects of obesity, therefore improving the use of calf circumference with higher rates of anastomotic leaks. Furthermore, they showed that
as a marker of low muscle mass.51 This is important because of the myosteatosis was an independent predictor of overall and severe
high prevalence of obesity and the fact that excess subcutaneous complications55 (Figure 7A). Reduced disease‐free survival was also
adipose tissue provides unreliable findings, as it is very difficult to observed for patients with myosteatosis compared with those without
identify low calf circumference in patients with excess body weight. myosteatosis (55.2% vs 87.2%, respectively; P = 0.007).55
Using a simple approach derived from a population‐representative Myosteatosis has been associated with poor survival and
cohort of adults of all ages, Gonzalez et al.51 proposed body surgical complications in other surgical contexts, including pancre-
mass index (BMI)–related adjustment factors. After measuring calf atic, gastric, and colorectal surgery, as shown in Figure 7A and B
circumference in patients with a BMI beyond the reference range and described by Murnane et al.55 In patients undergoing
2
(18.5–24.9 kg/m ), 3, 7, and 12 cm for patients within the over- pancreaticoduodenectomy, myosteatosis was associated with an
weight, obesity class I, and obesity class II categories, respectively, increased rate of major complications (P = 0.035) but was not
should be subtracted from the measured calf circumference. After associated with disease‐free or overall survival.65 However, low
that, the adjusted value can be compared with reference standards. muscle radiodensity analyzed as a continuous variable was
The authors51 proposed <34 cm for men and <33 cm for women as associated with survival.65 Notably, the combined phenotype of
markers of moderately low calf circumference, and <32 cm for men myosteatosis and low muscle mass has been associated with worse
and <31 cm for women as markers of severely low calf circumfer- clinical outcomes, as shown previously.48,66
ence. These were values for White individuals, with small differences From a methodological perspective, standardized CT protocols,
in cutoff values by ethnicity (decimal places). For individuals with a with intravenous contrast in the portal venous phase, are required to
low BMI (<18.5 kg/m2), an addition of 4 cm (to the measured value) is ensure that measures of skeletal muscle radiodensity are consistent
suggested. However, most of the participants from that sample were and comparable between CT images.67 Contrast enhancement, and
young and healthy, contrary to what is commonly observed among the phase of the scan, can significantly influence skeletal muscle
surgical patients. As such, adjustments in patients with low BMI density values. On a related note, the use of single‐muscle
(<18.5 kg/m2) may not be required in clinical settings, and the actual approaches when evaluating CT images is discouraged and may lead
measured calf circumference value should be used (ie, without to underestimation of the prevalence of myoesteatosis.68
adjustment) to compare with reference values in this population. The use of CT imaging for body composition analysis is of special
Therefore, adjustment factors would only need to be applied for importance in surgical oncology, as these images are readily available
surgical patients with a BMI of ≥25 kg/m2. Of note, correction values from medical records of most patients, acquired for the original
for edema have also been proposed by Ishida et al,52 which include purpose of cancer diagnosis and surveillance.47,69 However, prospec-
subtracting 2 cm for men and 1.6 cm for women from the measured tive, single images can be obtained for the purpose of body
calf circumference value when edema is present. composition analysis, to minimize radiation exposure. In fact, we
are aware of single‐slice CT imaging being specifically acquired in
routine clinical practice (coding, billing, and reporting in medical
Computerized tomography record) in some centers worldwide (including Harvard hospitals
[P. Wischmeyer, MD, personal communication]). This technique takes
The use of computerized tomography (CT) images for muscle mass minimal time to perform and exposes patients to less radiation than a
assessment has transformed the importance of body composition in chest x‐ray.
clinical settings, including the surgical patients. Low muscle mass has Importantly, automated segmentation is modernizing the use of
been associated with surgical complications, increased length of CT images in clinical settings, providing a time‐efficient, clinic‐
hospital stay, greater need for rehabilitation, and poorer survival, friendly, and accurate assessment of muscle and adipose tissues.70
48,53
among others. In addition to muscle mass, muscle radiodensity is Cespedes‐Feliciano et al.70 and Beetz et al.71 mentioned several
reflective of fat infiltration into muscle, or myosteatosis, and is an publications exploring automated and semiautomated software for
54–56
emerging powerful predictor of patient outcomes. CT‐derived body composition analysis and the need for their
Muscle radiodensity has been less studied in the surgical context. evaluation in large patient data sets.70 Cespedes‐Feliciano et al.70
Studies exploring myosteatosis in the surgical patient suggest a strong evaluated a commercially available semiautomated software and
association with postoperative morbidity and mortality.48,55,57–64 compared it with manual segmentation in nearly 6000 images of
48
Xiao et al. explored the significance of myosteatosis in patients patients with breast or colorectal cancer. Average Jaccard scores
undergoing colonic resection, using a large database from an (Jaccard similarity coefficient or intersection over union score) and
integrated healthcare system. Patients with myosteatosis were more intraclass correlation coefficients exceeded 90%, with only 1%–2%
likely to remain hospitalized 7 days or longer after surgery, had higher underestimation for muscle mass.70
risk of overall mortality, and had higher odds of developing major The first picture archiving and communication system
complications (Figure 7A and B). Murnane et al.55 studied patients (PACS)–integrated artificial intelligence–based software has been
undergoing radical surgery for esophageal and gastric cancer. More developed.71 This approach eliminates the need for manual
 19412444, 2023, S1, Downloaded from https://aspenjournals.onlinelibrary.wiley.com/doi/10.1002/jpen.2420 by Cochrane Colombia, Wiley Online Library on [16/02/2023]. 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
JOURNAL OF PARENTERAL AND ENTERAL NUTRITION | S61

F I G U R E 7 (A) Multivariate odds ratio from studies exploring the association of myosteatosis with poor clinical outcomes (excluding survival)
in the surgical context. (B) Multivariate hazard ratio for shorter survival related to myosteatosis from various surgical studies. All studies
compared patients with myosteatosis against patients without myosteatosis (reference; odds ratio or hazard ratio: 1). All values presented are
significant (P < 0.05). Conduit complications defined in the cited study as clinically silent fistulae, clinically important leaks that required
interventions, and frank gastric necroses.

identification of the landmark of interest for muscle mass analysis (eg, association between abnormal body composition and long‐term
the third lumbar vertebra [L3]), facilitating the process of automated survival.
segmentation that was lacking from previously available software and Finally, a new approach is the fully automated, multiple‐tissue,
semiautomated programs. As such, the software eliminates the need multiple‐organ, three‐dimensional segmentation and assessment by a
to anonymize DICOM images during the extraction process from commercially available software (Figure 8).73 In this software program
PACS to a second computer where body composition analysis that runs locally on a desktop or laptop computer, all available cross‐
would take place. Time and effort are substantially reduced when sectional axial slices obtained from a CT image are analyzed and
71
automation is used. Machine learning algorithms have been used to segmented, and each slice is annotated by its vertebral level. A
automatically detect the L3 vertebra. Using this approach, Kim et al.72 complete automated analysis of the volume of all body composition
selected preoperative CT images for body composition analysis in components such as skeletal muscle, visceral adipose tissue, sub-
patients with gastric cancer receiving gastrectomy and reported an cutaneous adipose tissue, and intramuscular adipose tissue by each
 19412444, 2023, S1, Downloaded from https://aspenjournals.onlinelibrary.wiley.com/doi/10.1002/jpen.2420 by Cochrane Colombia, Wiley Online Library on [16/02/2023]. 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
S62 | PRADO ET AL.

F I G U R E 8 Three‐dimensional, fully automated body composition imaging analysis from computerized tomography (CT) using DAFS—the data
analysis facilitation suite by Voronoi Health Analytics Inc, Canada.73 DAFS can segment any field of view of CT images from head to toe from
contrast and noncontrast images and low‐dose and conventional‐dose images in both adults and children. The software is fully automated and
provides detailed quality assessment interfaces. AI, artificial intelligence; Adapted with permission from Voronoi Health Analytics Inc, Canada.

slice is completed. Thus, organs such as liver and spleen can also be most often used, standardized values considering sex, age, and BMI
quantified. Machine learning algorithms can be used subsequently to can also be used.77
predict individual patient outcomes. Not only is this revolutionizing the Although phase angle has long been recognized as an important
assessment of body composition beyond one cross‐sectional area and and independent predictor of postoperative complications,78 it has
specific compartments (ie, skeletal muscle), but it also makes not been widely used in the context of postoperative morbidity in the
the use of this technique an accessible and rapid approach for surgical setting.79 However, the growing availability of BIA machines
implementation and integration into clinical practice. Consequently, providing this measurement and/or raw values for its calculation has
this can substantially accelerate the use of CT body composition revitalized the importance of phase angle.
imaging for clinical use, including in surgical and nutrition planning. Phase angle has been more recently associated as a marker of
Examples of open‐source software for manual and/or semiautomated muscle mass and function.80 These may be due to changes in muscle
segmentation include Horos (Horos Project), 3D Slicer (3D Slicer size, density, architecture, fiber types, mitochondrial function, and
project), ImageJ (National Institutes of Health), and CoreSlicer and abnormal hydration shifts, among others.80 Its sensitivity to capture
procedures for image analysis using selected software available changes over a short period of time81 is especially attractive and
74–76
elsewhere. should be explored in interventional studies in surgical settings.
The use of phase angle to predict perioperative risk in patients
undergoing surgery for cancer has been reviewed by Matthews
Bioelectrical impedance analysis—Phase angle et al.79 Twelve studies were included in their analysis that concluded
that BIA may be used in the perioperative period to predict risk of
Phase angle is derived from raw measurements of resistance and complications following elective surgery for cancer. Notably, phase
reactance obtained from bioelectrical impedance analysis (BIA). It is a angle was the BIA measurement more consistently associated
measure of the shift that occurs when the electrical current passes with predicting outcomes than derived BIA estimates. This could be
through the cell membrane; the shift is smaller in “sick” cell related to phase angle being a more direct biomarker (ie, raw vs
membranes because of a delay in current transmission, leading to a predicted measurement) and more reflective of cell and likely muscle
lower phase angle. Therefore, phase angle is reflective of cell health (including quality). The authors hypothesized that phase angle
membrane integrity, intracellular and extracellular water balance, may be identifying nonobvious cases of malnutrition in which
and consequently, overall health status. Although raw values are metabolic derangement is present.
 19412444, 2023, S1, Downloaded from https://aspenjournals.onlinelibrary.wiley.com/doi/10.1002/jpen.2420 by Cochrane Colombia, Wiley Online Library on [16/02/2023]. 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
JOURNAL OF PARENTERAL AND ENTERAL NUTRITION | S63

Newer studies have explored phase angle in surgical settings. can be used for additional assessment of other body composition
Petrolo et al.82 used bioimpedance spectroscopy to measure phase compartments, including appendicular lean soft tissue (often called
angle in a small sample of patients after pancreaticoduodenectomy or appendicular skeletal muscle mass). DXA has also been used in
total pancreatectomy. They observed a significant reduction in phase different surgical contexts.91–94
angle in early postoperative days, suggestive of cell loss or reduced The use of D3 creatine dilution95 can also be explored in these
cell integrity. The concurrent decrease in extracellular water was patients, although this method is currently more feasible for research
suggestive of an increase in extracellular volume related to a settings owing to the need for isotope data analysis. As such, its relevance
decrease in body cell mass.82 and practicality in clinical settings remain to be determined.96
In patients undergoing cardiac surgery, low preoperative phase Finally, magnetic resonance imaging (MRI) is making its way to clinical
angle was an indicator of poor nutrition status and was associated use on a fee‐for‐service, private‐use basis in selected countries. Rapid,
with higher rates and risk of postoperative morbidity (odds ratio whole‐body, MRI‐based body composition profiling is now available at
[OR] = 2.50; 95% CI, 1.18–5.29; P = 0.016) after cardiac surgery. selected diagnostic facilities in North America and Europe. Quantification
Researchers also observed a tendency toward longer length of of skeletal muscle volume and fat infiltration is possible (in addition to
83
hospital stay (>14 days) for patients with low phase angle. Previous liver fat fraction, as well as visceral and abdominal subcutaneous adipose
studies have found similar associations of phase angle as a predictor tissue volumes, Figure 9A). The process involves a specific MR scanning
of in‐hospital mortality (hazard ratio = 1.3; 95% CI, 1.07–1.40; protocol (typical 8 min of scanning time). Thereafter, the acquired images
P = 0.003) in patients undergoing cardiac surgery.84 are transferred to a central location using a secure cloud‐based service, in
which automated body composition profiling is conducted using a
proprietary approach97; the generated body composition profile report is
Ultrasound subsequently sent back to the diagnostic imaging facility with the body
composition measurements (Figure 9B). The personalized report given to
Ultrasound is an up‐and‐coming technique with important advan- the customer provides information on whether individuals have low or
tages (Figure 5) for use in surgical settings. The availability of pocket‐ high amounts of the specific body composition compartment, as well as a
size devices is perhaps the most notable advancement of this personalized control group to put the target patient into context of
method. In a small study in healthy participants, measurements of someone with a similar BMI, with references based on the UK Biobank
muscle thickness and architecture were similar between standard and MRI sex‐specific reference database (Figure 9A and B). In addition to
85
pocket‐size ultrasound. research settings, these images can be potentially used in clinical care,
Ultrasound has been used in the surgical setting. Bury et al.86 although affordability and accessibility are limitations to be considered.
explored its use to assess short‐term substantial changes in Notably, research protocols and analyses with a greater number of body
quadriceps muscle layer thickness in critically ill surgical patients. In composition variables are also available (Figure 9C). High reproducibility
a study including patients in the surgical and medical ward, a single and precision have been reported,98 as well as clinically relevant
ultrasound measuring point at the thigh (ie, muscle thickness) plus outcomes97 and magnitudes of exercise‐induced increases in muscle
sex, weight, and height were used in a model to predict CT‐assessed volume and reduction of fat infiltration after an 8‐week resistance‐
87
muscle mass (at the L3 level). training program.99
Notably, although there is a growing interest in using ultrasound
as an indirect marker of muscle glycogen concentration (from
echogenicity), its validity is questionable. We refer the reader to Frailty
another publication discussing this issue.88 Ultrasound echogenicity
can nonetheless be used as a surrogate for muscle quality surrogate, Frailty is a state of systemic increased vulnerability across multiple
similarly to CT radiodensity.89 organ systems that compromises the ability to respond to
Finally, protocols are evolving and so is our understanding of stressors.24,100 Assessment of frailty is part of the preoperative care
assessment and analytical approaches of this technique. Recent evidence of older surgical patients and an important predictor of morbidity,
highlights the need for establishing the number and location of mortality, or new disability after surgery.101,102 A preoperative
measurement sites, and the development of body composition predictive diagnosis of frailty can determine the cost/benefit of surgery, long‐
equations, which may be able to bypass the lack of normative data.90 term independence and productivity, and the value of undertaking
targeted interventions to reduce morbidity and mortality.100
Commonly used frailty assessment tools have been discussed
Additional methods elsewhere.28 In the surgical setting, a variety of tools has been used,
such as the modified 5‐Item Frailty Index (mFI‐5),103 the Geriatric
Additional body composition techniques can be explored for body Nutritional Risk Index,104 the Rockwood Clinical Frailty Scale,105 the
composition assessment during the perioperative period. For example, Edmonton Frail Scale,106 and the Fried frailty criteria.107 In regard to
most clinical centers have a dual‐energy X‐ray absorptiometry (DXA) screening tools, newer, easy‐to‐use instruments such as the Sunfrail
scan available for the assessment of bone health (osteoporosis). This (http://www.sunfrail.eu/), consistent with the biopsychosocial model, is
 19412444, 2023, S1, Downloaded from https://aspenjournals.onlinelibrary.wiley.com/doi/10.1002/jpen.2420 by Cochrane Colombia, Wiley Online Library on [16/02/2023]. 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
S64 | PRADO ET AL.

F I G U R E 9 Magnetic resonance imaging (MRI) analysis from AMRA Medical. (A) Whole‐body images separated by water (left) and adipose
tissue (right), based on MRI processed and analyzed using AMRA Medical machine learning and automation methods; available at selected
diagnostic imaging facilities. (B) AMRA BCP Scan (Body Composition Profile) sample report with body composition measurements quantified and
compared with reference values and a personalized control group (blue field in the bar plots). (C) Sample adipose tissue– and water‐separated
MR images for research from AMRA Medical. Adapted with permission from AMRA Medical.
 19412444, 2023, S1, Downloaded from https://aspenjournals.onlinelibrary.wiley.com/doi/10.1002/jpen.2420 by Cochrane Colombia, Wiley Online Library on [16/02/2023]. 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
JOURNAL OF PARENTERAL AND ENTERAL NUTRITION | S65

now available,108 although its use in surgery is yet to be explored. Chelsia Gillis, Paul E. Wischmeyer, Chet A. Morrison, and Dileep N. Lobo
Practical and valid approaches can facilitate the screening of frailty, contributed to the interpretation of the data. Carla M. Prado, Katherine L.
identifying the need to observe individuals using the Comprehensive Ford, Maria C. Gonzalez, Lisa C. Murnane, Chelsia Gillis, Paul E.
Geriatric Assessment.108 Wischmeyer, Chet A. Morrison, and Dileep N. Lobo drafted the
Ligthart‐Melis et al.7 discussed the prevalence of prefrailty, frailty, manuscript. All authors critically revised the manuscript, agree to be fully
sarcopenia, risk of malnutrition, and malnutrition in older hospitalized accountable for ensuring the integrity and accuracy of the work, and read
patients, which included surgical patients, using a systematic review/ and approved the final manuscript.
meta‐analysis approach. Among the 10 included studies, they reported
a higher prevalence of frailty (71%) compared with commonly CONFLIC T OF INTERESTS
observed prevalence in community‐dwelling older individuals. The Carla M. Prado reports receiving honoraria and/or paid consultancy
ORs between and the overlapping prevalence of prefrailty and (risk of) from Abbott Nutrition, Nutricia, Nestlé Health Science, Fresenius
malnutrition were 5.8% and 50%, respectively.7 Kabi, Pfizer, and AMRA Medical. Maria C. Gonzalez reports receiving
The Society for Perioperative Assessment and Quality Improve- honoraria for invited educational talks from Abbott Nutrition and
ment (SPAQI) proposed practical steps for clinicians to assess and Nestlé Health Science. Lisa C. Murnane has received honorarium
address frailty in older patients who require elective intermediate‐ or from Fresenius Kabi and Nestlé Health Science, outside of the
high‐risk surgery.109 In their workflow diagram, screening for frailty submitted work. Chelsia Gillis reports receiving honoraria for invited
may lead to the identification of high‐risk patients, which should educational talks from Abbott Nutrition, Nestlé Health Science, and
subsequently undergo frailty assessment using the Comprehensive Fresenius Kabi. Paul E. Wischmeyer reports receiving investigator‐
Geriatric Assessment tool. Screening and assessment should occur days initiated grant funding from National Institutes of Health, Depart-
to weeks before surgery and so should the intervention for those ment of Defense, Canadian Institutes of Health Research, Abbott
diagnosed with frailty. The proposed intervention pathway highlights Nutrition, Baxter, Cardinal Health, and Fresenius. Paul E. Wischmeyer
the importance of continuing care weeks after surgery (8 weeks), which has served as a consultant to Abbott Nutrition, Fresenius, Baxter,
involves nutrition, physical exercise, and psychological intervention. Cardinal Health, and Nutricia, for research related to this work. Paul
This is in line with the wildfire analogy29 mentioned earlier: early and E. Wischmeyer has received unrestricted gift donations for nutrition
continued assessment and intervention are critical for these patients. research from Musclesound and DSM. Paul E. Wischmeyer has
received honoraria or travel expenses for CME lectures on improving
nutrition care from Abbott Nutrition, Baxter, Danone‐Nutricia, and
CONCL US I ONS Nestlé. Katherine L. Ford, Chet A. Morrison, and Dileep N. Lobo have
no conflict of interests to declare. The content of this article was
Evaluating nutrition risk and status is essential to predict and mitigate presented during the course, Comprehensive Nutrition Therapy:
surgical outcomes. Novel to nascent approaches are the future of Tactical Approaches in 2022 (March 25, 2022), which was organized
diagnosing perioperative malnutrition objectively and guiding perio- by the ASPEN Physician Engagement Committee and preceded the
perative therapy toward optimal standard of care. ASPEN 2022 Nutrition Science & Practice Conference. The author(s)
Early and continued nutrition and frailty screening and assessment received a modest monetary honorarium. The conference recordings
are encouraged to better identify patients who are at extremely high were posted to the ASPEN eLearning Center https://aspen.
surgical risk. Widespread implementation of malnutrition and frailty digitellinc.com/aspen/store/6/index/6.
screening/assessment will, therefore, help with the shared decision‐
making process. These assessments are especially informative in cases ORC I D
when surgery may cause more harm than benefit, such as higher than Carla M. Prado http://orcid.org/0000-0002-3609-5641
expected morbidity, mortality, prolonged recovery process, and the Katherine L. Ford http://orcid.org/0000-0002-8620-9360
unlikelihood of returning to self‐care or near‐normal activities. Further- M. Cristina Gonzalez http://orcid.org/0000-0002-3901-8182
more, the assessment of nutrition status can lead to targeted interven- Chelsia Gillis http://orcid.org/0000-0002-0615-5922
tions that may improve short‐ and long‐term patient outcomes, including Paul E. Wischmeyer http://orcid.org/0000-0002-3369-7911
mitigating muscle loss. Chet A. Morrison http://orcid.org/0000-0001-8677-9534
Dileep N. Lobo http://orcid.org/0000-0003-1187-5796
A U T H O R C O N TR I B U T I O N S
Carla M. Prado contributed to the conception and design of the research. RE F ER EN CES
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2. Wischmeyer PE, Carli F, Evans DC, et al. American Society for
Gonzalez, Lisa C. Murnane, Chelsia Gillis, Paul E. Wischmeyer, Chet A. enhanced recovery and perioperative quality initiative joint consensus
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 19412444, 2023, S1, Downloaded from https://aspenjournals.onlinelibrary.wiley.com/doi/10.1002/jpen.2420 by Cochrane Colombia, Wiley Online Library on [16/02/2023]. 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
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