The prevalence and outcomes of frailty in older cancer patients: a systematic review
Open accessAbstract
Background Frailty is a state of vulnerability to poor resolution of homeostasis following a stressor event, such as chemotherapy or cancer surgery. Better knowledge of the epidemiology of frailty could help drive a global cancer care strategy for older people. The aim of this review was to establish the prevalence and outcomes of frailty and pre-frailty in older cancer patients.Methods Observational studies that reported data on the prevalence and/or outcomes of frailty in older cancer patients with any stage of solid or haematological malignancy were considered. We searched Medline, CINAHL, Cochrane Library, EMBASE, Web of Science, Allied and Complementary medicine, Psychinfo and ProQuest (1 January 1996 to 30 June 2013). The primary outcomes were prevalence of frailty, treatment-related side-effects, unplanned hospitalization and mortality. Risk of bias was assessed using the Newcastle-Ottawa checklist.Results Data from 20 studies evaluating 2916 participants are included. The median reported prevalence of frailty and pre-frailty was 42% (range 6%-86%) and 43% (range 13%-79%), respectively. A median of 32% (range 11%-78%) of patients were classified as fit. Frailty was independently associated with increased all-cause mortality [adjusted 5-year hazard ratio (HR) 1.87, 95% confidence interval (CI) 1.36-2.57]. There was evidence of increased risk of postoperative mortality for both frailty (adjusted 30-day HR 2.67, 95% CI 1.08-6.62) and pre-frailty (adjusted HR 2.33, 95% CI 1.20-4.52). Treatment complications were more frequent in those with frailty, including intolerance to cancer treatment (adjusted odds ratio 4.86, 95% CI 2.19-10.78) and postoperative complications (adjusted 30-day HR 3.19, 95% CI 1.68-6.04).Conclusions More than half of older cancer patients have pre-frailty or frailty and these patients are at increased risk of chemotherapy intolerance, postoperative complications and mortality. The findings of this review support routine assessment of frailty in older cancer patients to guide treatment decisions, and the development of multidisciplinary geriatric oncology services.
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A formal DAFI has not previously been applied to older cancer patients receiving chemotherapy.
“A formal Deficit Accumulation Frailty Index has not previously been applied to older cancer patients receiving chemotherapy.(19)”
From Frailty as determined by a comprehensive geriatric assessment-derived deficit-accumulation index in older patients with cancer who receive chemotherapy (2016) · cites this paper as [19]
Clinicians and investigators find a summary measure useful for stratification and outcome prediction.
“Though the individual components of the CGA are needed to direct specific interventions, clinicians and investigators find having a summary measure useful for stratification and outcome prediction (19).”
From Frailty as determined by a comprehensive geriatric assessment-derived deficit-accumulation index in older patients with cancer who receive chemotherapy (2016) · cites this paper as [19]
Cites
Frailty in Older Adults: Evidence for a Phenotype
Fried, L. P., Tangen, C. M., Walston, J., Newman, A. B., Hirsch, C., Gottdiener, J., Seeman, T., Tracy, R., Kop, W. J., Burke, G., et al. (2001) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/56.3.m146 · Cited by 24,907 · see citing works
Stroup, D. F. (2000) · JAMA · doi:10.1001/jama.283.15.2008 · Cited by 20,623 · see citing works
(2014) · Medical Entomology and Zoology · Cited by 17,633 · see citing works
Clegg, A., Young, J., Iliffe, S., Rikkert, M. O., & Rockwood, K. (2013) · The Lancet · doi:10.1016/s0140-6736(12)62167-9 · Cited by 9,503 · see citing works
Self-citationPrevalence of frailty in community-dwelling older persons: a systematic review
Collard, R. M., Boter, H., Schoevers, R. A., & Oude Voshaar, R. C. (2012) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2012.04054.x · Cited by 3,073 · see citing works
Underrepresentation of Patients 65 Years of Age or Older in Cancer-Treatment Trials
Hutchins, L. F., Unger, J. M., Crowley, J. J., Coltman, C. A., & Albain, K. S. (1999) · New England Journal of Medicine · doi:10.1056/nejm199912303412706 · Cited by 2,171 · see citing works
Wildiers, H. P. M. W., Heeren, P., Puts, M. T. E., Topinková, E., Janssen-Heijnen, M. L. G., Extermann, M., Falandry, C., Artz, A. S., Brain, E. G. C., Colloca, G. A., et al. (2014) · Journal of Clinical Oncology · doi:10.1200/jco.2013.54.8347 · Cited by 1,854 · see citing works
Proposed classification of complications of surgery with examples of utility in cholecystectomy.
Clavien, P., Sanabria, J. R., & Strasberg, S. M. (1992) · PubMed · Cited by 1,629 · see citing works
Prevalence and 10‐Year Outcomes of Frailty in Older Adults in Relation to Deficit Accumulation
Song, X., Mitnitski, A., & Rockwood, K. (2010) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2010.02764.x · Cited by 1,104 · see citing works
Ellis, G., Whitehead, M. A., Robinson, D., O'Neill, D., & Langhorne, P. (2011) · BMJ · doi:10.1136/bmj.d6553 · Cited by 1,068 · see citing works
The common biology of cancer and ageing
Finkel, T., Serrano, M., & Blasco, M. A. (2007) · Nature · doi:10.1038/nature05985 · Cited by 988 · see citing works
Talarico, L., Chen, G., & Pazdur, R. (2004) · Journal of Clinical Oncology · doi:10.1200/jco.2004.02.175 · Cited by 727 · see citing works
Quoix, E., Zalcman, G., Oster, J.-P., Westeel, V., Pichon, E., Lavolé, A., Dauba, J., Debieuvre, D., Souquet, P.-J., Bigay-Game, L., et al. (2011) · The Lancet · doi:10.1016/s0140-6736(11)60780-0 · Cited by 566 · see citing works
Rostoft, S., Nesbakken, A., Slaaen, M., Skovlund, E., Audisio, R. A., Johannessen, H., Bakka, A. O., & Wyller, T. B. (2009) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2009.11.002 · Cited by 456 · see citing works
Cohen, M. E., Bilimoria, K. Y., Ko, C. Y., & Hall, B. L. (2009) · Journal of the American College of Surgeons · doi:10.1016/j.jamcollsurg.2009.01.043 · Cited by 364 · see citing works
Use of Geriatric Assessment for Older Adults in the Oncology Setting: A Systematic Review
Puts, M. T. E., Hardt, J., Monette, J., Girre, V., Springall, E., & Alibhai, S. M. H. (2012) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djs285 · Cited by 335 · see citing works
Comprehensive geriatric assessment – a guide for the non‐specialist
Welsh, T. J., Gordon, A. L., & Gladman, J. R. F. (2013) · International Journal of Clinical Practice · doi:10.1111/ijcp.12313 · Cited by 290 · see citing works
Cancer incidence in the United Kingdom: projections to the year 2030
Mistry, M., Parkin, D. M., Ahmad, A. S., & Sasieni, P. D. (2011) · British Journal of Cancer · doi:10.1038/bjc.2011.430 · Cited by 277 · see citing works
An update on a systematic review of the use of geriatric assessment for older adults in oncology
Puts, M. T. E., dos Santos, B. S., Hardt, J., Monette, J., Girre, V., Atenafu, E. G., Springall, E., & Alibhai, S. M. H. (2013) · Annals of Oncology · doi:10.1093/annonc/mdt386 · Cited by 254 · see citing works
Tan, K., Kawamura, Y., Tokomitsu, A., & Tang, T. (2011) · The American Journal of Surgery · doi:10.1016/j.amjsurg.2011.08.012 · Cited by 253 · see citing works
Mohile, S. G., Bylow, K. A., Dale, W., Dignam, J. J., Martin, K., Petrylak, D. P., Stadler, W. M., & Rodin, M. B. (2007) · Cancer · doi:10.1002/cncr.22495 · Cited by 253 · see citing works
The cancer survival gap between elderly and middle-aged patients in Europe is widening
Quaglia, A., Tavilla, A., Shack, L., Brenner, H., Janssen-Heijnen, M. L. G., Allemani, C., Colonna, M., Grande, E., Grosclaude, P., & Vercelli, M. (2009) · European Journal of Cancer · doi:10.1016/j.ejca.2008.11.028 · Cited by 223 · see citing works
Meta-analysis of Observational Studies
Greenwood, D. C. (2012) · Springer eBooks · doi:10.1007/978-94-007-3024-3_10 · Cited by 180 · see citing works
Clough‐Gorr, K. M., Stuck, A. E., Thwin, S. S., & Silliman, R. A. (2009) · Journal of Clinical Oncology · doi:10.1200/jco.2009.23.5440 · Cited by 177 · see citing works
The Accumulation of Deficits with Age and Possible Invariants of Aging
Mitnitski, A. B., Mogilner, A. J., MacKnight, C., & Rockwood, K. J. (2002) · The Scientific World JOURNAL · doi:10.1100/tsw.2002.861 · Cited by 175 · see citing works
Comprehensive Geriatric assessment and its clinical impact in oncology
Maas, H. A. A. M., Janssen-Heijnen, M. L. G., Rikkert, M. G. M. O., & Wymenga, A. N. M. (2007) · European Journal of Cancer · doi:10.1016/j.ejca.2007.08.002 · Cited by 172 · see citing works
Hamaker, M. E., Vos, A. G., Smorenburg, C. H., de Rooij, S. E., & Munster, B. C. V. (2012) · The Oncologist · doi:10.1634/theoncologist.2012-0186 · Cited by 167 · see citing works
Frailty: An outcome predictor for elderly gynecologic oncology patients
Courtney-Brooks, M. B., Tellawi, A. R., Scalici, J. M., Duska, L., Jazaeri, A. A., Modesitt, S. C., & Cantrell, L. A. (2012) · Gynecologic Oncology · doi:10.1016/j.ygyno.2012.04.019 · Cited by 143 · see citing works
Baitar, A., Fraeyenhove, F. V., Vandebroek, A., Droogh, E. D., Galdermans, D., Mebis, J., & Schrijvers, D. L. A. L. (2012) · Journal of Geriatric Oncology · doi:10.1016/j.jgo.2012.08.001 · Cited by 135 · see citing works
Wedding, U., Ködding, D., Pientka, L., Steinmetz, H. T., & Schmitz, S. (2007) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2007.05.001 · Cited by 125 · see citing works
Puts, M. T. E., Monette, J., Girre, V., Pepe, C., Monette, M., Assouline, S. E., Panasci, L., Basik, M., Miller, W. H., Batist, G., et al. (2010) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2010.04.003 · Cited by 122 · see citing works
Identifying an accurate pre-screening tool in geriatric oncology
Kellen, E., Bulens, P., Deckx, L., Schouten, H. C., van Dijk, M., Verdonck, I., & Buntinx, F. (2010) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2009.12.002 · Cited by 99 · see citing works
A comparison of two pre-operative frailty measures in older surgical cancer patients
Rostoft, S., Rønning, B., Hurria, A., Skovlund, E., Jordhøy, M. S., Nesbakken, A., & Wyller, T. B. (2011) · Journal of Geriatric Oncology · doi:10.1016/j.jgo.2011.09.002 · Cited by 95 · see citing works
Clough‐Gorr, K. M., Thwin, S. S., Stuck, A. E., & Silliman, R. A. (2011) · European Journal of Cancer · doi:10.1016/j.ejca.2011.06.016 · Cited by 88 · see citing works
Owusu, C., Koroukian, S. M., SCHLUCHTER, M. D., Bakaki, P. M., & Berger, N. A. (2011) · Journal of Geriatric Oncology · doi:10.1016/j.jgo.2010.12.002 · Cited by 84 · see citing works
Rétornaz, F., Monette, J., Batist, G., Monette, M., Sourial, N., Small, D., Caplan, S. N., Wan-Chow-Wah, D., Puts, M. T. E., & Bergman, H. (2008) · The Journals of Gerontology Series A · doi:10.1093/gerona/63.5.518 · Cited by 73 · see citing works
Bylow, K. A., Hemmerich, J. A., Mohile, S. G., Stadler, W. M., Sajid, S., & Dale, W. (2011) · Urology · doi:10.1016/j.urology.2010.11.024 · Cited by 70 · see citing works
Lawler, M., Selby, P. J., Aapro, M., et al. (2014) · BMJ · doi:10.1136/bmj.g1614 · Cited by 66 · see citing works
Self-citationComparison of two frailty screening tools in older women with early breast cancer
Molina-Garrido, M. J., & Guillén‐Ponce, C. (2010) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2010.06.004 · Cited by 55 · see citing works
Luciani, A., Dottorini, L., Battisti, N. M. L., Bertuzzi, C., Caldiera, S., Floriani, I., Zonato, S., Ferrari, D., & Foa, P. (2012) · Annals of Oncology · doi:10.1093/annonc/mds471 · Cited by 30 · see citing works
Infancy of an Australian geriatric oncology program—characteristics of the first 200 patients
To, T. H. M., Okera, M., Prouse, J., Prowse, R. J., & Singhal, N. (2010) · Journal of Geriatric Oncology · doi:10.1016/j.jgo.2010.07.003 · Cited by 24 · see citing works
Who needs a comprehensive geriatric assessment? A French Onco-Geriatric Screening tool (OGS)
Valéro, S., Migeot, V., Bouche, G., Raban, N., Roullet, B., Dreyfus, B., Paccalin, M., & Tourani, J. M. (2011) · Journal of Geriatric Oncology · doi:10.1016/j.jgo.2010.12.001 · Cited by 20 · see citing works
Geriatric assessment in older lung cancer patients
Maddison, C., Irving, L., Lim, K., et al. (2018) · VU Research Portal · Cited by 1 · see citing works
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Cohen, H. J., Smith, D., Sun, C., Tew, W., Mohile, S. G., Owusu, C., Klepin, H. D., Gross, C. P., Lichtman, S. M., Gajra, A., et al. (2016) · Cancer · doi:10.1002/cncr.30269 · Cited by 203 · see citing works
Guerard, E. J., Deal, A. M., Chang, Y., Williams, G. R., Nyrop, K. A., Pergolotti, M., Muss, H. B., Sanoff, H. K., & Lund, J. L. (2017) · Journal of the National Comprehensive Cancer Network · doi:10.6004/jnccn.2017.0122 · Cited by 168 · see citing works
Kadambi, S., Loh, K. P., Dunne, R., Magnuson, A., Maggiore, R., Zittel, J., Flannery, M., Inglis, J., Gilmore, N., Mohamed, M., et al. (2020) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-020-0421-z · Cited by 149 · see citing works
Screening for frailty in Canada’s health care system: A time for action
Muscedere, J., Andrew, M. K., Bagshaw, S. M., Estabrooks, C., Hogan, D., Holroyd-Leduc, J., Howlett, S., Lahey, W., Maxwell, C., McNally, M., et al. (2016) · Canadian Journal on Aging / La Revue canadienne du vieillissement · doi:10.1017/s0714980816000301 · Cited by 112 · see citing works
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Sattar, S., Haase, K. R., Lee, K., & Campbell, K. L. (2024) · Current Opinion in Supportive & Palliative Care · doi:10.1097/spc.0000000000000685 · Cited by 3 · see citing works
- Authors
- Handforth, C., Clegg, A., Young, C., Simpkins, S., Seymour, M. T., Selby, P. J., & Young, J.
- Affiliations
- Leeds Teaching Hospitals NHS Trust (GB)
- University of Leeds (GB)
- Corresponding author
- Handforth, C.
- Venue
- Annals of Oncology
- Publisher
- Elsevier BV
- Published
- 2015-06
- Volume
- 26
- Issue
- 6
- Pages
- 1091-1101
- ISSN
- 0923-7534 (ISSN-L)
- OpenAlex
- W2159230388
- Cited by
- 1,048
- References
- 43
- Citations by year
- 2026: 105 · 2025: 118 · 2024: 151 · 2023: 128 · 2022: 137 · 2021: 108 · 2020: 72 · 2019: 67 · 2018: 49 · 2017: 53 · 2016: 41 · 2015: 16 · 2014: 1 · 2012: 1
- FWCI
- 3.16
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Annals of Oncology (publishedVersion)
- PubMed (publishedVersion)
- White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (submittedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- National Institute for Health and Care Research (NF-SI-0509-10020)
- Topics
- Health Sciences › Medicine › Geriatrics and Gerontology › Frailty in Older Adults
- Health Sciences › Medicine › Physiology › Nutrition and Health in Aging
- Health Sciences › Medicine › Geriatrics and Gerontology › Pharmaceutical Practices and Patient Outcomes
- Keywords
- frailty, pre-frailty, elderly cancer patients, frailty prevalence, all-cause mortality, postoperative mortality, chemotherapy intolerance, treatment side effects, postoperative complications, frailty assessment, geriatric oncology, hematologic malignancies, solid tumors, multidisciplinary care, frailty screening, frailty interventions, quality of life, functional status
- MeSH terms
- Age Factors, Aged, Aged, 80 and over, Antineoplastic Agents, Female, Humans, Male, Neoplasms, Postoperative Complications, Predictive Value of Tests, Risk Factors, Geriatric Assessment, Comorbidity, Prevalence, Odds Ratio, Frail Elderly, Treatment Outcome
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