Validation of GLIM malnutrition criteria in cancer patients undergoing major abdominal surgery: A large-scale prospective study

  • Author Footnotes
    1 Shanjun Tan and Junjie Wang contributed equally to this work.
    Shanjun Tan
    Footnotes
    1 Shanjun Tan and Junjie Wang contributed equally to this work.
    Affiliations
    Department of General Surgery/Shanghai Clinical Nutrition Research Center, Zhongshan Hospital, Fudan University, Shanghai, China
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  • Author Footnotes
    1 Shanjun Tan and Junjie Wang contributed equally to this work.
    Junjie Wang
    Footnotes
    1 Shanjun Tan and Junjie Wang contributed equally to this work.
    Affiliations
    Department of General Surgery/Shanghai Clinical Nutrition Research Center, Zhongshan Hospital, Fudan University, Shanghai, China
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  • Feng Zhou
    Affiliations
    Department of General, Visceral and Transplant Surgery, University Hospital Heidelberg, Heidelberg, Germany
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  • Min Tang
    Affiliations
    Department of Radiology, Zhongshan Hospital, Fudan University, Shanghai, China
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  • Jiahao Xu
    Affiliations
    Department of General Surgery/Shanghai Clinical Nutrition Research Center, Zhongshan Hospital, Fudan University, Shanghai, China
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  • Yanni Zhang
    Affiliations
    Department of General Surgery/Shanghai Clinical Nutrition Research Center, Zhongshan Hospital, Fudan University, Shanghai, China
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  • Mingyue Yan
    Affiliations
    Department of General Surgery/Shanghai Clinical Nutrition Research Center, Zhongshan Hospital, Fudan University, Shanghai, China
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  • Shuhao Li
    Affiliations
    Department of General Surgery/Shanghai Clinical Nutrition Research Center, Zhongshan Hospital, Fudan University, Shanghai, China
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  • Zhige Zhang
    Affiliations
    Department of General Surgery/Shanghai Clinical Nutrition Research Center, Zhongshan Hospital, Fudan University, Shanghai, China
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  • Guohao Wu
    Correspondence
    Corresponding author. Department of General Surgery/Shanghai Clinical Nutrition Research Center, Zhongshan Hospital, Fudan University, 180 Fenglin Road, Xuhui District, Shanghai 200032, China.
    Affiliations
    Department of General Surgery/Shanghai Clinical Nutrition Research Center, Zhongshan Hospital, Fudan University, Shanghai, China
    Search for articles by this author
  • Author Footnotes
    1 Shanjun Tan and Junjie Wang contributed equally to this work.
Published:January 12, 2022DOI:https://doi.org/10.1016/j.clnu.2022.01.010

      Summary

      Background & aims

      The Global Leadership Initiative on Malnutrition (GLIM) is a new framework to evaluate nutritional status. It has been validated mostly by retrospective studies, which often failed to follow the framework as recommended due to their retrospective nature. This study aims to validate GLIM with a large prospective study and investigate its role in predicting short-term surgical outcomes.

      Methods

      Patients who underwent abdominal surgery for digestive cancer in our center were prospectively included between January 2020 and December 2020. Data collected included demographic information, clinical and pathological information, lab results, and computed tomography scans. Muscle strength, physical performances, quality of life and cancer symptom burden were evaluated upon admission. Multiple tools for nutritional risk screening were used. Nutritional status was evaluated with Subjective Global Assessment (SGA) and GLIM. Postoperative outcomes collected included return of gastrointestinal function, postoperative length of stay, complications, 30-day readmission and 30-day mortality.

      Results

      A total of 1115 patients were evaluated with GLIM criteria. Inter-rater reliability was good [k = 0.76, 95% confidence interval (CI): 0.72–0.80]. The accuracy of GLIM diagnosis compared to the semi-gold standard SGA varied with the screening method used. GLIM with MNA-SF screening [area under the curve (AUC): 0.78] and GLIM without screening (AUC: 0.77) were the two most accurate protocols, and there was no significant difference between the two from a clinical perspective. GLIM can predict preoperative nutritional status, functional status, symptom burden and quality of life. It can also predict complications after surgery [odds ratio (OR) = 2.31, 95% CI: 1.67–3.21], especially infection related complications (OR = 2.19, 95% CI: 1.38–3.49) and wound healing related complications (OR = 2.54, 95% CI: 1.38–4.71).

      Conclusions

      GLIM malnutrition criteria showed good inner-rater reliability and moderate agreement with SGA. GLIM can be used to predict preoperative nutritional status, functional status, cancer related symptoms, and quality of life. It can also predict postoperative outcomes especially complications that are related to infection and wound healing. In surgical candidates, the screening process could potentially be skipped so that GLIM assessment can be faster, more accessible, and more sensitive.

      Keywords

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      References

        • Sung H.
        • Ferlay J.
        • Siegel R.L.
        • Laversanne M.
        • Soerjomataram I.
        • Jemal A.
        • et al.
        Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
        CA A Cancer J Clin. 2021; 71: 209-249
        • Marshall K.M.
        • Loeliger J.
        • Nolte L.
        • Kelaart A.
        • Kiss N.K.
        Prevalence of malnutrition and impact on clinical outcomes in cancer services: a comparison of two time points.
        Clin Nutr. 2019; 38: 644-651
        • Arends J.
        • Baracos V.
        • Bertz H.
        • Bozzetti F.
        • Calder P.C.
        • Deutz N.E.P.
        • et al.
        ESPEN expert group recommendations for action against cancer-related malnutrition.
        Clin Nutr. 2017; 36: 1187-1196
        • Williams D.G.A.
        • Molinger J.
        • Wischmeyer P.E.
        The malnourished surgery patient: a silent epidemic in perioperative outcomes?.
        Curr Opin Anaesthesiol. 2019; 32: 405-411
        • Cederholm T.
        • Jensen G.L.
        • Correia M.
        • Gonzalez M.C.
        • Fukushima R.
        • Higashiguchi T.
        • et al.
        GLIM criteria for the diagnosis of malnutrition - a consensus report from the global clinical nutrition community.
        Clin Nutr. 2019; 38: 1-9
        • de van der Schueren M.A.E.
        • Keller H.
        • Cederholm T.
        • Barazzoni R.
        • Compher C.
        • Correia M.
        • et al.
        Global Leadership Initiative on Malnutrition (GLIM): guidance on validation of the operational criteria for the diagnosis of protein-energy malnutrition in adults.
        Clin Nutr. 2020; 39: 2872-2880
        • Charlson M.
        • Szatrowski T.P.
        • Peterson J.
        • Gold J.
        Validation of a combined comorbidity index.
        J Clin Epidemiol. 1994; 47: 1245-1251
        • Leong D.P.
        • Teo K.K.
        • Rangarajan S.
        • Kutty V.R.
        • Lanas F.
        • Hui C.
        • et al.
        Reference ranges of handgrip strength from 125,462 healthy adults in 21 countries: a prospective urban rural epidemiologic (PURE) study.
        J Cachexia Sarcopenia Muscle. 2016; 7: 535-546
        • Zhang S.
        • Tan S.
        • Jiang Y.
        • Xi Q.
        • Meng Q.
        • Zhuang Q.
        • et al.
        Sarcopenia as a predictor of poor surgical and oncologic outcomes after abdominal surgery for digestive tract cancer: a prospective cohort study.
        Clin Nutr. 2019; 38: 2881-2888
        • Yin L.
        • Lin X.
        • Li N.
        • Zhang M.
        • He X.
        • Liu J.
        • et al.
        Evaluation of the global leadership initiative on malnutrition criteria using different muscle mass indices for diagnosing malnutrition and predicting survival in lung cancer patients.
        J Parenter Enteral Nutr. 2021; 45: 607-617
        • Guralnik J.M.
        • Simonsick E.M.
        • Ferrucci L.
        • Glynn R.J.
        • Berkman L.F.
        • Blazer D.G.
        • et al.
        A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission.
        J Gerontol. 1994; 49: M85-M94
      1. ATS statement: guidelines for the six-minute walk test.
        Am J Respir Crit Care Med. 2002; 166: 111-117
        • Fayers P.
        • Aaronson N.K.
        • Bjordal K.
        • Groenvold M.
        • Curran D.
        • Bottomley A.
        EORTC QLQ-C30 scoring manual: European organisation for Research and treatment of cancer.
        2001
        • Cleeland C.S.
        • Mendoza T.R.
        • Wang X.S.
        • Chou C.
        • Harle M.T.
        • Morrissey M.
        • et al.
        Assessing symptom distress in cancer patients: the M.D. Anderson Symptom Inventory.
        Cancer. 2000; 89: 1634-1646
        • Dindo D.
        • Demartines N.
        • Clavien P.A.
        Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey.
        Ann Surg. 2004; 240: 205-213
        • Martin L.
        • Senesse P.
        • Gioulbasanis I.
        • Antoun S.
        • Bozzetti F.
        • Deans C.
        • et al.
        Diagnostic criteria for the classification of cancer-associated weight loss.
        J Clin Oncol. 2015; 33: 90-99
        • Kondrup J.
        • Allison S.P.
        • Elia M.
        • Vellas B.
        • Plauth M.
        ESPEN guidelines for nutrition screening 2002.
        Clin Nutr. 2003; 22: 415-421
        • Rubenstein L.Z.
        • Harker J.O.
        • Salvà A.
        • Guigoz Y.
        • Vellas B.
        Screening for undernutrition in geriatric practice: developing the short-form mini-nutritional assessment (MNA-SF).
        J Gerontol A Biol Sci Med Sci. 2001; 56: M366-M372
        • Stratton R.J.
        • Hackston A.
        • Longmore D.
        • Dixon R.
        • Price S.
        • Stroud M.
        • et al.
        Malnutrition in hospital outpatients and inpatients: prevalence, concurrent validity and ease of use of the 'malnutrition universal screening tool' ('MUST') for adults.
        Br J Nutr. 2004; 92: 799-808
        • Wischmeyer P.E.
        • Carli F.
        • Evans D.C.
        • Guilbert S.
        • Kozar R.
        • Pryor A.
        • et al.
        American society for enhanced recovery and perioperative quality initiative joint consensus statement on nutrition screening and therapy within a surgical enhanced recovery pathway.
        Anesth Analg. 2018; 126: 1883-1895
        • Detsky A.S.
        • McLaughlin J.R.
        • Baker J.P.
        • Johnston N.
        • Whittaker S.
        • Mendelson R.A.
        • et al.
        What is subjective global assessment of nutritional status?.
        J Parenter Enteral Nutr. 1987; 11: 8-13
        • Argiles J.M.
        • Betancourt A.
        • Guardia-Olmos J.
        • Pero-Cebollero M.
        • Lopez-Soriano F.J.
        • Madeddu C.
        • et al.
        Validation of the CAchexia SCOre (CASCO). Staging cancer patients: the use of miniCASCO as a simplified tool.
        Front Physiol. 2017; 8
        • Argiles J.M.
        • Lopez-Soriano F.J.
        • Toledo M.
        • Betancourt A.
        • Serpe R.
        • Busquets S.
        The cachexia score (CASCO): a new tool for staging cachectic cancer patients.
        J Cachexia Sarcopenia Muscle. 2011; 2: 87-93
        • Maeda K.
        • Ishida Y.
        • Nonogaki T.
        • Mori N.
        Reference body mass index values and the prevalence of malnutrition according to the Global Leadership Initiative on Malnutrition criteria.
        Clin Nutr. 2020; 39: 180-184
        • Fearon K.
        • Strasser F.
        • Anker S.D.
        • Bosaeus I.
        • Bruera E.
        • Fainsinger R.L.
        • et al.
        Definition and classification of cancer cachexia: an international consensus.
        Lancet Oncol. 2011; 12: 489-495
        • Chen L.K.
        • Woo J.
        • Assantachai P.
        • Auyeung T.W.
        • Chou M.Y.
        • Iijima K.
        • et al.
        Asian working group for sarcopenia: 2019 consensus update on sarcopenia diagnosis and treatment.
        J Am Med Dir Assoc. 2020; 21: 300-307.e2
        • Brito J.E.
        • Burgel C.F.
        • Lima J.
        • Chites V.S.
        • Saragiotto C.B.
        • Rabito E.I.
        • et al.
        GLIM criteria for malnutrition diagnosis of hospitalized patients presents satisfactory criterion validity: a prospective cohort study.
        Clin Nutr. 2021; 40: 4366-4372
        • Rosnes K.S.
        • Henriksen C.
        • Hoidalen A.
        • Paur I.
        Agreement between the GLIM criteria and PG-SGA in a mixed patient population at a nutrition outpatient clinic.
        Clin Nutr. 2021; 40: 5030-5037
        • Xu J.Y.
        • Zhu M.W.
        • Zhang H.
        • Li L.
        • Tang P.X.
        • Chen W.
        • et al.
        A cross-sectional study of GLIM-defined malnutrition based on new validated calf circumference cut-off values and different screening tools in hospitalised patients over 70 Years old.
        J Nutr Health Aging. 2020; 24: 832-838
        • Team R.C.
        R: a language and environment for statistical computing.
        R Foundation for Statistical Computing, 2020
        • Subirana I.
        • Sanz H.
        • Vila J.
        Building bivariate tables: the {compareGroups} package for {R.
        J Stat Software. 2014; 57: 1-16
        • Daly L.
        • Dolan R.
        • Power D.
        • Ni Bhuachalla E.
        • Sim W.
        • Fallon M.
        • et al.
        The relationship between the BMI-adjusted weight loss grading system and quality of life in patients with incurable cancer.
        J Cachexia Sarcopenia Muscle. 2020; 11: 160-168
        • Zhang X.
        • Tang M.
        • Zhang Q.
        • Zhang K.P.
        • Guo Z.Q.
        • Xu H.X.
        • et al.
        The GLIM criteria as an effective tool for nutrition assessment and survival prediction in older adult cancer patients.
        Clin Nutr. 2021; 40: 1224-1232
        • Skeie E.
        • Tangvik R.J.
        • Nymo L.S.
        • Harthug S.
        • Lassen K.
        • Viste A.
        Weight loss and BMI criteria in GLIM's definition of malnutrition is associated with postoperative complications following abdominal resections - results from a National Quality Registry.
        Clin Nutr. 2020; 39: 1593-1599
        • Allard J.P.
        • Keller H.
        • Gramlich L.
        • Jeejeebhoy K.N.
        • Laporte M.
        • Duerksen D.R.
        GLIM criteria has fair sensitivity and specificity for diagnosing malnutrition when using SGA as comparator.
        Clin Nutr. 2020; 39: 2771-2777
        • Coussens L.M.
        • Werb Z.
        Inflammation and cancer.
        Nature. 2002; 420: 860-867
        • Fearon K.
        • Arends J.
        • Baracos V.
        Understanding the mechanisms and treatment options in cancer cachexia.
        Nat Rev Clin Oncol. 2013; 10: 90-99
        • Han J.
        • Meng Q.Y.
        • Shen L.
        • Wu G.H.
        Interleukin-6 induces fat loss in cancer cachexia by promoting white adipose tissue lipolysis and browning.
        Lipids Health Dis. 2018; 17: 8
        • Vagnildhaug O.M.
        • Blum D.
        • Wilcock A.
        • Fayers P.
        • Strasser F.
        • Baracos V.E.
        • et al.
        The applicability of a weight loss grading system in cancer cachexia: a longitudinal analysis.
        J Cachexia Sarcopenia Muscle. 2017; 8: 789-797
        • Helminen H.
        • Luukkaala T.
        • Saarnio J.
        • Nuotio M.S.
        Predictive value of the mini-nutritional assessment short form (MNA-SF) and nutritional risk screening (NRS2002) in hip fracture.
        Eur J Clin Nutr. 2019; 73: 112-120
        • Raslan M.
        • Gonzalez M.C.
        • Dias M.C.G.
        • Nascimento M.
        • Castro M.
        • Marques P.
        • et al.
        Comparison of nutritional risk screening tools for predicting clinical outcomes in hospitalized patients.
        Nutrition. 2010; 26: 721-726
        • Lobo D.N.
        • Gianotti L.
        • Adiamah A.
        • Barazzoni R.
        • Deutz N.E.P.
        • Dhatariya K.
        • et al.
        Perioperative nutrition: recommendations from the ESPEN expert group.
        Clin Nutr. 2020; 39: 3211-3227
        • Correia M.I.
        • Waitzberg D.L.
        The impact of malnutrition on morbidity, mortality, length of hospital stay and costs evaluated through a multivariate model analysis.
        Clin Nutr. 2003; 22: 235-239
        • Reisinger K.W.
        • van Vugt J.L.
        • Tegels J.J.
        • Snijders C.
        • Hulsewe K.W.
        • Hoofwijk A.G.
        • et al.
        Functional compromise reflected by sarcopenia, frailty, and nutritional depletion predicts adverse postoperative outcome after colorectal cancer surgery.
        Ann Surg. 2015; 261: 345-352
        • Maccio A.
        • Sanna E.
        • Neri M.
        • Oppi S.
        • Madeddu C.
        Cachexia as evidence of the mechanisms of resistance and tolerance during the evolution of cancer disease.
        Int J Mol Sci. 2021; 22
        • Cruz-Jentoft A.J.
        • Bahat G.
        • Bauer J.
        • Boirie Y.
        • Bruyere O.
        • Cederholm T.
        • et al.
        Sarcopenia: revised European consensus on definition and diagnosis.
        Age Ageing. 2019; 48: 16-31
        • Cederholm T.
        • Barazzoni R.
        A year with the GLIM diagnosis of malnutrition - does it work for older persons?.
        Curr Opin Clin Nutr Metab Care. 2021; 24: 4-9
        • Sanchez-Rodriguez D.
        • Locquet M.
        • Bruyère O.
        • Lengelé L.
        • Cavalier E.
        • Reginster J.Y.
        • et al.
        Prediction of 5-year mortality risk by malnutrition according to the GLIM format using seven pragmatic approaches to define the criterion of loss of muscle mass.
        Clin Nutr. 2021; 40: 2188-2199
        • De Groot L.M.
        • Lee G.
        • Ackerie A.
        • van der Meij B.S.
        Malnutrition screening and assessment in the cancer care ambulatory setting: mortality predictability and validity of the patient-generated subjective global assessment short form (PG-SGA SF) and the GLIM criteria.
        Nutrients. 2020; 12
        • van Bokhorst-de van der Schueren M.A.
        • Guaitoli P.R.
        • Jansma E.P.
        • de Vet H.C.
        Nutrition screening tools: does one size fit all? A systematic review of screening tools for the hospital setting.
        Clin Nutr. 2014; 33: 39-58