Abstract
Purpose
Malnutrition (MN) in cancer is common but underdiagnosed. Dietitian referrals may not occur until MN is established. We investigated cancer patient characteristics (demographics, nutritional status, and nutrition barriers) on referral to oncology dietitians. We also examined referral practices and prevalence of missed referral opportunities.
Methods
This was a naturalistic multi-site study of clinical practice. Data from consecutive referrals were collected in inpatient and outpatient settings. Demographics, nutritional status (weight, body mass index (BMI), weight loss in the preceding 3–6 months, oral intake, nutrition barriers), referral reasons, and use of screening were recorded. Missed opportunities for earlier referral were also noted.
Results
Two hundred patients were included (60% male, 51% inpatients). Half had gastrointestinal and hepatobiliary cancers. The majority were on antitumor treatment. Two-thirds had lost ≥ 5% body weight. Forty percent were overweight or obese. Seventy percent had ≥ 2 nutritional barriers. Most common nutrition barriers were anorexia, nausea, and early satiety. Greater weight loss and lower food intake were associated with ≥ 2 barriers. Weight loss was the most common referral reason. Screening was used in 35%. Referrals should have occurred sooner in nearly half (45%, n = 89).
Conclusions
Cancer patients were referred late to a dietitian, with multiple nutritional barriers. Most referrals were for established weight loss (WL). WL may be masked by pre-existing obesity. Almost half had missed earlier referral opportunities; screening was infrequent. Over one-quarter should have been re-referred sooner. There is a clear need for clinician education. Future research should investigate the optimal timing of dietitian referral and the best nutrition screening tools for use in cancer.
Similar content being viewed by others
Data availability
The authors confirm having full control of primary data and agree that Supportive Care in Cancer may review this data on request.
References
Muscaritoli M, Lucia S, Farcomeni A, Lorusso V, Saracino V, Barone C, Plastino F, Gori S, Magarotto R, Carteni G, Chiurazzi B, Pavese I, Marchetti L, Zagonel V, Bergo E, Tonini G, Imperatori M, Iacono C, Maiorana L, Pinto C, Rubino D, Cavanna L, Di Cicilia R, Gamucci T, Quadrini S, Palazzo S, Minardi S, Merlano M, Colucci G, Marchetti P (2017) Prevalence of malnutrition in patients at first medical oncology visit: the PreMiO study. Oncotarget 8(45):79884–79896. https://doi.org/10.18632/oncotarget.20168
Cederholm T, Jensen GL, Correia M, Gonzalez MC, Fukushima R, Higashiguchi T, Baptista G, Barazzoni R, Blaauw R, Coats AJS, Crivelli AN, Evans DC, Gramlich L, Fuchs-Tarlovsky V, Keller H, Llido L, Malone A, Mogensen KM, Morley JE, Muscaritoli M, Nyulasi I, Pirlich M, Pisprasert V, de van der Schueren MAE, Siltharm S, Singer P, Tappenden K, Velasco N, Waitzberg D, Yamwong P, Yu J, Van Gossum A, Compher C (2019) GLIM criteria for the diagnosis of malnutrition - a consensus report from the global clinical nutrition community. J Cachexia Sarcopenia Muscle 10(1):207–217. https://doi.org/10.1002/jcsm.12383
Bozzetti F, Mariani L, Lo Vullo S, Amerio ML, Biffi R, Caccialanza G, Capuano G, Correja I, Cozzaglio L, Di Leo A, Di Cosmo L, Finocchiaro C, Gavazzi C, Giannoni A, Magnanini P, Mantovani G, Pellegrini M, Rovera L, Sandri G, Tinivella M, Vigevani E (2012) The nutritional risk in oncology: a study of 1,453 cancer outpatients. Support Care Cancer 20(8):1919–1928. https://doi.org/10.1007/s00520-012-1387-x
Marshall KM, Loeliger J, Nolte L, Kelaart A, Kiss NK (2019) Prevalence of malnutrition and impact on clinical outcomes in cancer services: a comparison of two time points. Clin Nutr 38(2):644–651. https://doi.org/10.1016/j.clnu.2018.04.007
Pressoir M, Desne S, Berchery D, Rossignol G, Poiree B, Meslier M, Traversier S, Vittot M, Simon M, Gekiere JP, Meuric J, Serot F, Falewee MN, Rodrigues I, Senesse P, Vasson MP, Chelle F, Maget B, Antoun S, Bachmann P (2010) Prevalence, risk factors and clinical implications of malnutrition in French Comprehensive Cancer Centres. Br J Cancer 102(6):966–971. https://doi.org/10.1038/sj.bjc.6605578
Planas M, Alvarez-Hernandez J, Leon-Sanz M, Celaya-Perez S, Araujo K, Garcia de Lorenzo A (2016) Prevalence of hospital malnutrition in cancer patients: a sub-analysis of the PREDyCES(R) study. Support Care Cancer 24(1):429–435. https://doi.org/10.1007/s00520-015-2813-7
Arends J, Bachmann P, Baracos V, Barthelemy N, Bertz H, Bozzetti F, Fearon K, Hutterer E, Isenring E, Kaasa S, Krznaric Z, Laird B, Larsson M, Laviano A, Muhlebach S, Muscaritoli M, Oldervoll L, Ravasco P, Solheim T, Strasser F, de van der Schueren M, Preiser JC (2017) ESPEN guidelines on nutrition in cancer patients. Clin Nutr 36(1):11–48. https://doi.org/10.1016/j.clnu.2016.07.015
Ottery FD (1996) Definition of standardized nutritional assessment and interventional pathways in oncology. Nutrition 12(1 Suppl):S15–S19
Ryan AM, Power DG, Daly L, Cushen SJ, Ni Bhuachalla E, Prado CM (2016) Cancer-associated malnutrition, cachexia and sarcopenia: the skeleton in the hospital closet 40 years later. Proc Nutr Soc 75(2):199–211. https://doi.org/10.1017/s002966511500419x
Martin L, Kubrak C (2018) How much does reduced food intake contribute to cancer-associated weight loss? Curr Opin Support Palliat Care 12(4):410–419. https://doi.org/10.1097/spc.0000000000000379
Phillips K (2007) Thought for food: nutritional assessment of chemotherapy patients. Cancer Nurs Pract 6(5):25–30
Hanna L, Huggins CE, Furness K, Silvers MA, Savva J, Frawley H, Croagh D, Cashin P, Low L, Bauer J, Truby H, Haines T (2018) Effect of early and intensive nutrition care, delivered via telephone or mobile application, on quality of life in people with upper gastrointestinal cancer: study protocol of a randomised controlled trial. BMC Cancer 18(1):707. https://doi.org/10.1186/s12885-018-4595-z
Spiro A, Baldwin C, Patterson A, Thomas J, Andreyev HJ (2006) The views and practice of oncologists towards nutritional support in patients receiving chemotherapy. Br J Cancer 95(4):431–434. https://doi.org/10.1038/sj.bjc.6603280
National Collaborating Centre for Acute Care (2006) Nutrition support in adults oral nutrition support, enteral tube feeding and parenteral nutrition. National Collaborating Centre for Acute Care, London
(2014) Clinical nutrition guidelines of the French Speaking Society of Clinical Nutrition and Metabolism (SFNEP): summary of recommendations for adults undergoing non-surgical anticancer treatment. Dig Liver Dis 46(8):667–674. https://doi.org/10.1016/j.dld.2014.01.160
Fearon K, Strasser F, Anker SD, Bosaeus I, Bruera E, Fainsinger RL, Jatoi A, Loprinzi C, MacDonald N, Mantovani G, Davis M, Muscaritoli M, Ottery F, Radbruch L, Ravasco P, Walsh D, Wilcock A, Kaasa S, Baracos VE (2011) Definition and classification of cancer cachexia: an international consensus. Lancet Oncol 12(5):489–495. https://doi.org/10.1016/s1470-2045(10)70218-7
Gioulbasanis I, Martin L, Baracos VE, Thezenas S, Koinis F, Senesse P (2015) Nutritional assessment in overweight and obese patients with metastatic cancer: does it make sense? Ann Oncol 26(1):217–221. https://doi.org/10.1093/annonc/mdu501
Abbott J, Teleni L, McKavanagh D, Watson J, McCarthy AL, Isenring E (2016) Patient-Generated Subjective Global Assessment Short Form (PG-SGA SF) is a valid screening tool in chemotherapy outpatients. Support Care Cancer 24(9):3883–3887. https://doi.org/10.1007/s00520-016-3196-0
Elia M (2003) The MUST report. Nutritional screening of adults: a multidisciplinary responsibility. British Association for Parenteral and Enteral Nutrition, Redditch
Ferguson M, Capra S, Bauer J, Banks M (1999) Development of a valid and reliable malnutrition screening tool for adult acute hospital patients. Nutrition 15(6):458–464
Kondrup J, Rasmussen HH, Hamberg O, Stanga Z (2003) Nutritional risk screening (NRS 2002): a new method based on an analysis of controlled clinical trials. Clin Nutr 22(3):321–336
Ni Bhuachalla EB, Daly LE, Power DG, Cushen SJ, MacEneaney P, Ryan AM (2018) Computed tomography diagnosed cachexia and sarcopenia in 725 oncology patients: is nutritional screening capturing hidden malnutrition? J Cachexia Sarcopenia Muscle 9(2):295–305. https://doi.org/10.1002/jcsm.12258
Patel V, Romano M, Corkins MR, DiMaria-Ghalili RA, Earthman C, Malone A, Miller S, Sabino K, Wooley J, Guenter P (2014) Nutrition screening and assessment in hospitalized patients: a survey of current practice in the United States. Nutr Clin Pract 29(4):483–490. https://doi.org/10.1177/0884533614535446
Platek ME, Johnson J, Woolf K, Makarem N, Ompad DC (2015) Availability of outpatient clinical nutrition services for patients with cancer undergoing treatment at comprehensive cancer centers. J Oncol Pract 11(1):1–5. https://doi.org/10.1200/jop.2013.001134
Attar A, Malka D, Sabate JM, Bonnetain F, Lecomte T, Aparicio T, Locher C, Laharie D, Ezenfis J, Taieb J (2012) Malnutrition is high and underestimated during chemotherapy in gastrointestinal cancer: an AGEO prospective cross-sectional multicenter study. Nutr Cancer 64(4):535–542. https://doi.org/10.1080/01635581.2012.670743
Hebuterne X, Lemarie E, Michallet M, de Montreuil CB, Schneider SM, Goldwasser F (2014) Prevalence of malnutrition and current use of nutrition support in patients with cancer. JPEN J Parenter Enteral Nutr 38(2):196–204. https://doi.org/10.1177/0148607113502674
Baldwin C, McGough C, Norman AR, Frost GS, Cunningham DC, Andreyev HJ (2006) Failure of dietetic referral in patients with gastrointestinal cancer and weight loss. Eur J Cancer 42(15):2504–2509. https://doi.org/10.1016/j.ejca.2006.05.028
Davidson W, Teleni L, Muller J, Ferguson M, McCarthy AL, Vick J, Isenring E (2012) Malnutrition and chemotherapy-induced nausea and vomiting: implications for practice. Oncol Nurs Forum 39(4):E340–E345
de van der Schueren MAE, Laviano A, Blanchard H, Jourdan M, Arends J, Baracos VE (2018) Systematic review and meta-analysis of the evidence for oral nutritional intervention on nutritional and clinical outcomes during chemo (radio)therapy: current evidence and guidance for design of future trials. Ann Oncol 29(5):1141–1153. https://doi.org/10.1093/annonc/mdy114
Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET, Carbone PP (1982) Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol 5(6):649–655
(1995) Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee. World Health Organ Tech Rep Ser 854:1–452
Ipsos MRBI (2017) Healthy Ireland Survey. Dublin
Irish Nutrition and Dietetic Institution (2010) The Nutrition Support Reference Guide. Irish Nutrition and Dietetic Institution, Dublin
Ireland NCR (2018) Cancer factsheet overview & most common cancers. www.ncri.ie/sites/ncri/files/factsheets/Factsheet%20all%20cancers.pdf. Accessed 20 Dec 2018
Khalid U, Spiro A, Baldwin C, Sharma B, McGough C, Norman AR, Eisen T, O’Brien ME, Cunningham D, Andreyev HJ (2007) Symptoms and weight loss in patients with gastrointestinal and lung cancer at presentation. Support Care Cancer 15(1):39–46. https://doi.org/10.1007/s00520-006-0091-0
Martin L, Birdsell L, Macdonald N, Reiman T, Clandinin MT, McCargar LJ, Murphy R, Ghosh S, Sawyer MB, Baracos VE (2013) Cancer cachexia in the age of obesity: skeletal muscle depletion is a powerful prognostic factor, independent of body mass index. J Clin Oncol 31(12):1539–1547. https://doi.org/10.1200/jco.2012.45.2722
Cederholm T, Barazzoni R, Austin P, Ballmer P, Biolo G, Bischoff SC, Compher C, Correia I, Higashiguchi T, Holst M, Jensen GL, Malone A, Muscaritoli M, Nyulasi I, Pirlich M, Rothenberg E, Schindler K, Schneider SM, de van der Schueren MA, Sieber C, Valentini L, Yu JC, Van Gossum A, Singer P (2017) ESPEN guidelines on definitions and terminology of clinical nutrition. Clin Nutr 36(1):49–64. https://doi.org/10.1016/j.clnu.2016.09.004
Barajas Galindo DE, Vidal-Casariego A, Calleja-Fernandez A, Hernandez-Moreno A, Pintor de la Maza B, Pedraza-Lorenzo M, Rodriguez-Garcia MA, Avila-Turcios DM, Alejo-Ramos M, Villar-Taibo R, Urioste-Fondo A, Cano-Rodriguez I, Ballesteros-Pomar MD (2017) Appetite disorders in cancer patients: impact on nutritional status and quality of life. Appetite 114:23–27. https://doi.org/10.1016/j.appet.2017.03.020
Homsi J, Luong D (2007) Symptoms and survival in patients with advanced disease. J Palliat Med 10(4):904–909. https://doi.org/10.1089/jpm.2007.0004
Shahar S, Shirley N, Noah SA (2013) Quality and accuracy assessment of nutrition information on the Web for cancer prevention. Inform Health Soc Care 38(1):15–26
Boltong AG, Loeliger JM, Steer BL (2013) Using a public hospital funding model to strengthen a case for improved nutritional care in a cancer setting. Aust Health Rev 37(3):286–290. https://doi.org/10.1071/ah13010
Butterworth CE Jr (1974) The skeleton in the hospital closet. Nutr Today 9(2):4–8
Tobert CM, Mott SL, Nepple KG (2018) Malnutrition diagnosis during adult inpatient hospitalizations: analysis of a multi-institutional collaborative database of academic medical centers. J Acad Nutr Diet 118(1):125–131. https://doi.org/10.1016/j.jand.2016.12.019
Cox S, Powell C, Carter B, Hurt C, Mukherjee S, Crosby TD (2016) Role of nutritional status and intervention in oesophageal cancer treated with definitive chemoradiotherapy: outcomes from SCOPE1. Br J Cancer 115(2):172–177. https://doi.org/10.1038/bjc.2016.129
Yang YC, Lee MS, Cheng HL, Chou HY, Chan LC (2019) More frequent nutrition counseling limits weight loss and improves energy intake during oncology management: a longitudinal inpatient study in Taiwan. Nutr Cancer 71(3):452–460. https://doi.org/10.1080/01635581.2018.1516791
Acknowledgments
Study participants and dietitians.
Assisted with devising study concept and critically reviewed the study proposal: Dr. Martina Coen, Dr. Clare Corish, Catherine Corrigan, Roisin Gowan, Orla Haughey, Sinead Knox, Pauline Ui Dhuibhir
Critically reviewed the study proposal and facilitated dietitians’ involvement in study: Sinead Feehan, Una Gilligan, Dr. Lorraine Walsh
Collected data: Geraldine Guiry
Assisted with data entry: Shauna Kielthy
Provided guidance on and assistance with literature review: Fiona Lawler
Provided advice on statistical techniques: Centre for Support and Training in Analysis and Research (CSTAR), University College Dublin
Technical editing and proofreading: Kunal Kadakia, Aidan O’Donoghue, Niamh O’Donoghue, Gail M O’Neill
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical approval was granted by the research ethics committee at each hospital. Waiver of written consent was approved at three sites (Tallaght University Hospital, St. Vincent’s University Hospital, and St. Vincent’s Private Hospital). At two sites, written consent was sought (St. Luke’s Radiation Oncology Network and the Mater Private Mid-Western Regional Oncology Centre).
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Lorton, C.M., Griffin, O., Higgins, K. et al. Late referral of cancer patients with malnutrition to dietitians: a prospective study of clinical practice. Support Care Cancer 28, 2351–2360 (2020). https://doi.org/10.1007/s00520-019-05042-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00520-019-05042-2