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BMC geriatrics · 2025

The concept of multidimensional frailty in geriatric oncology: a systematic scoping review.

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Guo Y, Chen Y, Song S, Wang Z, Chen Y, Fu Z, Xu X, Xu Q, Ding L

Аннотация

BACKGROUND: One of the major challenges in geriatric oncology is to estimate the risk-benefit balance of any therapeutic proposal for each patient and frailty is one of the key components of Comprehensive Geriatric Assessment (CGA)and can also be assessed using stand-alone screening tools that predicts functional decline, treatment-related complications and mortality. This study aimed to provide an overview of the existing literature on the concept of multidimensional frailty in older adults with cancer, to clarify the dimensions included in multidimensional frailty, and the components of frailty under each dimension. METHODS: We followed the PRISMA guidelines and Arksey and O’Malley’s framework for scoping reviews, and the research question was developed according to the participants-concept-context (PCC) framework. We searched for literature related to multidimensional frailty concepts in the field of geriatric oncology published in multiple databases from database inception to December 2024 and used a data extraction form to extract and analyze the data RESULTS: The final scoping review included 25 studies, which were pooled to find that multidimensional frailty was a syndrome that centred on physical dimension, but also encompassing psychological, social, cognitive and oral dimensions. To better characterise multidimensional frailty, we summarised the components specific to frailty under each dimension. CONCLUSION: Our study provides a systematic overview of the concepts, dimensions, and components of multidimensional frailty in the field of geriatric oncology, which may contribute to the construction of an effective frailty assessment tool with a minimum number of dimensions to predict serious adverse events for older adults with cancer, as well as being important for the prevention and management of frailty, and for oncological rehabilitation. CLINICAL TRIAL NUMBER: not applicable.

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Introduction

According to the latest data from the International Agency for Research on Cancer (IARC), there were close to 19.98 million new cases of cancer in the year 2022, and the number of new cases is still increasing year by year [ 1 ]. With the aging of the world, there was approximately 12.94 million new cases of cancer in persons aged 60 years or older, accounting for 64.8% of all new cases [ 2 ]. In general, the prognosis of older adults with cancer is worse than that of younger patients. Nearly 50% of older adults with cancer experienced severe chemotherapy-related toxicity [ 3 ], and 60% experienced serious complications after surgery, including death [ 4 ]. One of the major challenges in geriatric oncology is to estimate the risk-benefit balance of any therapeutic proposal for each patient.

As aging is a highly heterogeneous process, therapeutic decisions must take into account the patient’s individual quality of aging, physical reserves, and potential risks of the planned treatment. Currently, to better identify individual heterogeneity, the International Society of Geriatric Oncology (SIOG) recommends a Comprehensive Geriatric Assessment (CGA) for older adults with cancer to systematically assess multiple domains of patient health, including functional status, cognition, nutrition, and psychological and social support [ 5 , 6 ]. Frailty is one of the key components of CGA and there are some stand-alone tools that screen for frailty to rapid identification of high-risk populations with inadequate physical reserve [ 7 ]. Some frailty screening tools have been validated in specific contexts to predict tolerance or risk of complications for a specific treatment, generally they are most appropriately used to identify older adults with cancer who would benefit from CGA [ 8 , 9 ]. Thus, for oncologists, conducting a frailty assessment can help to quickly identify whether a patient has sufficient reserve to tolerate a specific treatment [ 10 ], thereby assisting in the clinical development of a more individualized, risk-appropriate treatment plan [ 11 ].

Currently, a large number of frailty scales have been developed for the clinical identification of so-called “frail” patients in order to provide a more personalized treatment plan [ 12 , 13 ]. However, not all of these assessment tools clearly define frailty and the applicable population, resulting in a wide variety of assessment contents and items, chaotic tool usage, and inability to make comparisons among different studies. This has greatly hindered the further development of research in this field. Therefore, an accepted conceptual definition of frailty in geriatric oncology is essential.

However, the concept of “frailty” in geriatric oncology is still unclear. At present, the most widely used definition of frailty in the geriatric field are based on two models. One is the Frailty Cycle Model (FCM) proposed by Fried et al. in 2001, which defines frailty as “a biological syndrome of increased vulnerability of the organism due to a decline in the reserve of multiple physiological systems and a weakened resistance to stressors“ [ 14 ]. Another is the Frailty Index of Accumulative Deficits Model (FIAD) proposed by Rockwood and Mitnitski in 2001, which is based on the biological theory of pathogenesis and considers frailty to be “an age-related syndrome caused by the accumulation of a range of individual impairments and conditions that may increase the risk of adverse health outcomes“ [ 15 ]. However, as research continues, the FCM has been criticized for defining frailty in a way that only applies to the identification of physical frailty in the clinical setting and lacks assessment of cognitive and psycho-psychosocial aspects [ 16 ]. And the FIAD has been difficult to apply due to its multiple and time-consuming assessment items and the fact that it is administered by professionals. Subsequently, Gobbens et al. in 2010 proposed that frailty is “a dynamic state in which human function experiences loss in one or more domains (physical, psychological, social) due to the influence of a range of variables and increases the risk of adverse outcomes” based on the Integral Conceptual Model of Frailty [ 17 ]. Based on the Multidimensional Model, Ferrucci et al. in 2017 proposed that frailty is the absence of harmonious interaction between multiple domains (including genetic, biological, functional, cognitive, psychological and socio-economic domains), which ultimately leads to the dysregulation of human homeostasis [ 18 ]. At present, the latter two conceptual frameworks of frailty have gradually gained popularity. However, as far as the concept of multidimensional frailty, it remains unclear what dimensions its frailty encompasses and what the components of frailty are under each dimension.

Several previous reviews have addressed frailty in older adults with cancer, focusing primarily on screening tools [ 7 ], prevalence [ 19 ], clinical outcomes [ 12 ], or the predictive value of frailty assessments in oncology care [ 9 ]. However, these reviews have not systematically explored the conceptual definitions, dimensional structures, and dimension-specific components of multidimensional frailty within this population. Given the increasing recognition that frailty is a multidimensional construct, beyond purely physical aspects, and that a clear understanding of its dimensions is critical for valid assessment and intervention, there remains a gap in the literature regarding how frailty is defined and operationalized in geriatric oncology across its multiple dimensions.

Therefore, this scoping review was conducted to provide a comprehensive overview of the literature on multidimensional frailty in older adults with cancer, with the goal of identifying how frailty is conceptualized and what specific dimensions and components have been included across studies. This work seeks to inform future research, assessment development, and clinical application in geriatric oncology.

Methods

Research design

We used the scoping review approach, following the Preferred Reporting Items for Systematic reviews and Meta-Analysis extended for Scoping Reviews (PRISMA-ScR) checklist [ 20 ], to systematically synthesize concepts. Scoping reviews sit between narrative and systematic reviews [ 21 ] and are a useful methodology to develop a comprehensive overview of existing evidence in a particular field. Freytag et.al [ 22 ] defined a scoping review as“a quick summary of key concepts, primary sources of information, and types of literature and information (evidence) available in a research area”. Their main goal is to identify gaps in the research while providing an overview of a wide range of information to inform future research.

We conducted the scoping review mainly following Arksey and OMalley’s methodological framework [ 22 ], which involves five-step process: (1) identifying the research question; (2) identifying relevant studies; (3) screening studies; (4) extracting the data; and (5) summarizing and reporting the results. In addition, participants-concept-context (PCC) framework [ 23 ] was in the research question identification, Levac et al.‘s extension for optimizing the Arksey and O’Malley framework were also referenced in the study screening, data extraction, and results summary sections to enhance the systematicity and rigor of the review [ 24 ]. Because PROSPERO does not normally accept scoping review registrations (it mainly accepts systematic review), we did not register or publish on a public platform. However, we did develop an initial protocol for internal use before this review was conducted.

Research question identification

We developed the research questions of this scoping review based on participants-concept-context (PCC) framework [ 23 ] recommended by PRISMA-ScR.

P:Older adults with cancer (aged 60 years or older)

C:Multidimensional frailty, studies that assess any of frailty possible dimensions or components.

C:Older adults undergoing treatment for various types of cancer.

The research question for this scoping review was: “How is multidimensional frailty conceptualised in the field of geriatric oncology? Specifically, what possible dimensions and components are included?”.

Relevant literature identification

Two independent researchers conducted a comprehensive literature search of PubMed, Web of Science, Embase, CINAHL, Scopus, ProQuest, PsycINFO, China Knowledge Resource Integrated Database (CNKI), Wanfang, Weipu and SinoMed. The search terms were created based on the combination of Medical Subject Headings (MeSH) and free terms, and the literature search formula consists of two parts, the first of which was frailty or other possible dimensions of frailty; the second was neoplasm or other manifestations of neoplasm; as shown below: (frailty or frail* or frailty syndrome or debilit* or multidimensional frailty or physical frailty or psychological frailty or social frailty or cognitive frailty or oral frailty) AND (neoplasm or neoplas* or cancer* or tumor* or malignanc* or carcinoma or oncology or CA). In addition, reference lists of all relevant articles were manually searched to identify additional studies. The languages of the literature were limited to English and Chinese. The timeframe for the search was from database inception to December, 2024. The search strategy was provided in supplementary material. Our search strategy was designed in collaboration with university research librarians. All selected documents were saved in Endnote software.

Studies selection

Inclusion criteria for the literature: (1) The study was conducted in a cancer population aged 60 years or older. (2) The study explored frailty as a multidimensional concept or examined any of its possible dimensions or components.

Exclusion criteria for literature: (1) Duplicate publications. (2) Full-text literature unavailable after contacting the authors. (3) Letters, case reports and conference papers.

We imported the results of the literature search into Endnote and removed duplicates. Two researchers identified potentially relevant studies by screening the titles, abstracts, and keywords of the identified studies. Afterwards, they compared the initial results of this review to reach a consensus. The same two researchers independently screened the full-text articles based on the inclusion and exclusion criteria of the literature. Any disagreement between the two authors regarding literature selection was resolved by the third researcher to reach consensus.

Data extraction

Characteristics of eligible studies were extracted according to a pre-specified data extraction form, including authors, year, country or region, study design, sample size, primary tumor site, frailty definition, dimensions, components and measuring instruments. All researchers jointly developed the extraction details based on the JBI extraction template [ 24 ]. Information was extracted independently by 2 researchers. Any inconsistencies were resolved by consulting a third researcher. In addition, if data required clarification or key information was missing, the authors of the relevant study were contacted.

Data synthesis and analysis

Concepts, definitions, dimensions and components involving frailty were entered into a data extraction table for narrative synthesis. We manually grouped and evaluated these concepts, definitions, dimensions and components to derive a comprehensive definition of frailty, as well as the dimensions it encompasses, the frequency of appearance of each dimension, and to synthesize and analyze the components of frailty under the corresponding dimensions. The discussion group for data synthesis and analysis consisted of PhDs, professors, and clinical workers from our team who have long been dedicated to the field of frailty (including 3 PhDs, 1 doctoral supervisor and 2 clinical workers with 8 years of experience in oncology), all of whom are also authors of this article.

Results

Characteristics of the included publications

The initial search resulted in 5878 articles, of which 3 were added after additional citation review. 2920 articles remained after eliminating duplicate articles. By reading titles and abstracts, 163 articles were initially screened for full review and detailed assessment. Of these, 138 articles did not meet the eligibility criteria, and a total of 25 articles were ultimately included in the qualitative analysis. The process of screening studies according to the PRISMA guidelines is shown in Fig. 1 .

Fig. 1 PRISMA-ScR flowchart for the study selection process
Fig. 1 PRISMA-ScR flowchart for the study selection process

Twenty-five eligible articles were published between 2014 and 2024, of which 9 (36.0%) used a cross-sectional design [ 25 – 33 ], 9 cases (36.0%) used a longitudinal design [ 34 – 42 ], and 7 cases (28.0%) used theoretical analyses [ 43 – 49 ]. 6 (36.2%) were conducted in America [ 30 , 40 , 45 – 48 ], 3 in France [ 31 , 41 , 49 ], 9 in China [ 25 – 27 , 29 , 33 , 35 – 37 , 44 ], 4 in Japan [ 28 , 34 , 38 , 39 ], and the remaining 3 respectively in Germany [ 43 ], Italy [ 42 ], and India [ 32 ]. Table 1 described the characteristics of the included articles.

Table 1
Characteristics of included articles
N/A = Not Applicable or Not Available; ADLs : Activities of Daily Living; IADLs : Instrumental activities of daily living; CCI : Charlson comorbidity Index; GFI : Groningen Frailty Indicator; FP : Frailty phenotype; MoCA : Montreal cognitive assessment; EORTC : European Organization for Research and Treatment of Cancer Quality of Life Questionnaire; GA : Geriatric assessment; CGA : Comprehensive geriatric assessment; CFAI : Comprehensive Frailty Assessment Instrument; G8 : Geriatric 8; FI : Frailty Index

Authors (year)CountryResearch design (sample size)Primary tumor siteDefinition of frailtyDimensions of frailtyComponents of frailtyMeasuring Instruments
Wu et al. [ 25 ] (2024)ChinaCross-sectional ( n = 181)Digestive System TumorsFrailty is a multidimensional syndrome in which the organism suffers from multi-system organ dysfunction, reduced physiological reserve, increased vulnerability, and reduced resistance to stress.Physical frailty, cognitive frailty, psychological frailty and social frailtyPhysical frailty: (i) physical performance, (ii) functional status, (iii) hearing and eyesight, (iv) nutrition, (v) polypharmacy. Cognitive frailty: (i) memory Psychological frailty: (i) mood and (ii) emotion Social frailty: (i) social role, (ii) social relationsGFI
Mizuta et al.[ 34 ] (2024)JapanProspective cohort ( n = 208/70)gastrointestinal cancerSocial frailty, which reflects the social domain of frailty, is defined as a continuum of being at risk of losing or having lost social and general resources, activities, or abilities essential for fulfilling one or more basic social needs in life.Social frailty(i)going out less frequently, (ii) rarely visiting friends, (iii)feeling unhelpful to friends or family, (iv) living alone, and (v) not talking with someone every dayMakizako Social Frailty Index
Li et al. [ 26 ] (2024)ChinaCross-sectional ( n = 372)lung cancerCognitive frailty represents a heterogeneous clinical condition where physical frailty (PF) coexists with mild cognitive impairment (MCI), excluding other dementia types such as Alzheimer’s disease.Cognitive frailtyPhysical frailty: (i) involuntary weight loss, (ii) reduced grip strength, (iii) fatigue, (iv) decline in physical activity, and (v) slow walking speed; Mild cognitive impairment: (i) attention and concentration, (ii) executive function, (iii) memory, (iv) language, (v) visual structural skills, (vi) abstract thinking, (vii) numeracy and (viii) orientationFP + MoCA
Ho et al. [ 27 ] (2023)ChinaCross-sectional( n = 293)Any malignant tumorsThe concept of cognitive frailty has been proposed by an international consensus group, which defined cognitive frailty as the coexistence of physical weakness and cognitive decline without any existing dementia or other related conditions.Cognitive frailtyPhysical frailty: (i) involuntary weight loss, (ii) reduced grip strength, (iii) fatigue, (iv) decline in physical activity, and (v) slow walking speed. Cognitive functioning decline: (i) perceived attention and (ii) memory impairments.FP + the EORTC QLQ-C30 cognitive functioning subscale
Teranishi et al. [ 28 ] (2023)JapanCross-sectional ( n = 60)Gastric cancerThe Japan Dental Association defined “oral frailty” as a series of phenomena where poor oral health leads to poor mental and physical functioning.Oral frailty(i) the number of natural teeth, (ii) chewing ability, (iii) articulatory oral motor skill, (iv) tongue pressure, (v) subjective difficulty in eating tough foods, and (vi) subjective difficulty in swallowing.Questionnaires regarding subjective oral health
Goede et al. [ 43 ] (2023)GermanyTheoretical Review (n/a)Any malignant tumorsFrailty is generally defined as an age-related clinical condition of increased vulnerability to acute endogenous or exogenous stressors.Multidimensional frailty(i) social status, (ii) physical function, (iii) nutrition, (iv) cognition, (v) emotion, (vi) co-morbidity and (vii) polypharmacy.GA
Pu et al. [ 35 ](2023)ChinaProspective cohort ( n = 1763)Any malignant tumorsFrailty is a clinical syndrome of diminished physiologic reserve that results in increased vulnerability to stressors.Physical frailty(i) involuntary weight loss, (ii) reduced grip strength, (iii) fatigue, (iv) decline in physical activity, and (v) slow walking speed.FP
Miao et al. [ 36 ] (2023)ChinaProspective, longitudinal ( n = 404)Gastric cancerN/APhysical frailty, psychological frailty and social frailtyPhysical frailty: (i) functional status, (ii) nutrition, (iii) physical performance, (iv) hearing and eyesight, (v) reduced grip strength, and (vi) fatigue. Psychological frailty: (i) cognition and (ii) mood Social frailty: (i) live alone, (ii) Someone to be around, and (iii) get help from othersTFI
Zhang et al. [ 29 ] (2022)ChinaCross-sectional ( n = 394)Colorectal cancerFrailty is recognized as a clinical syndrome that is independent of the normal aging process.Physical frailty, psychological frailty and social frailtyPhysical frailty: (i) functional status, (ii) nutrition, (iii) physical performance, (iv) hearing and eyesight, (v) reduced grip strength, and (vi) fatigue. Psychological frailty: (i) cognition and (ii) mood Social frailty: (i) live alone, (ii) Someone to be around, and (iii) get help from othersTFI
Ho et al. [ 37 ] (2022)ChinaProspective, longitudinal ( n = 234)solid cancer or lymphomaFrailty refers to a decrease in the reserve capacity of multiple systems of the body, which increases the risk of adverse health outcomes when stressful events occur and the body is unable to respond and most scholars define frailty as the exhibition of deficits in two or more dimensions.Multidimensional frailty(i) functional status, (ii) cognition, (iii) nutrition, (iv) psychological mood, (v) social support, (vi) polypharmacy, (vii) comorbidity, and (viii) history of falls.Comprehensive frailty assessment
Koll et al. [ 30 ] (2021)AmericaCross-sectional ( n = 394)Any malignant tumors other than skin cancerPhysical frailty is an important, “medical syndrome with multiple causes and contributors characterized by diminished strength, endurance, and reduced physiologic function that increases an individual’s vulnerability for developing increased dependency and/or death.Physical frailty(i) self-rated exhaustion, (ii) weakness, (iii) slow gait, and (iv) low physical activity.A modified 4-point (FP
Ono et al. [ 38 ] (2021)JapanProspective cohort ( n = 195)Gastrointestinal CancerSocial frailty has been described as a continuum that assesses the risk of losing social and general resources, activities, or abilities that are important for fulfilling basic social needs during an individual’s life span.Social frailty(i)going out less frequently, (ii) rarely visiting friends, (iii)feeling unhelpful to friends or family, (iv) living alone, and (v) not talking with someone every dayMakizako Social Frailty Index
Okumura et al. [ 39 ] (2020)JapanRetrospective cohort( n = 113/48)Gastrointestinal cancerN/ASocial frailty(i)going out less frequently, (ii) rarely visiting friends, (iii)feeling unhelpful to friends or family, (iv) living alone, and (v) not talking with someone every dayMakizako Social Frailty Index
Isaacs et al. [ 40 ] (2020)AmericaProspective cohort( n = 40)Multiple myelomaFrailty is a collective deterioration of multiple physical and physiological functions yielding a lower tolerance of stressors such as cancer and treatments.Physical frailty and Multidimensional frailtyPhysical frailty: (i) ADLs, (ii) IADLs, (iii) CCI) and (iv) age Physical frailty: (i)comorbidity, (ii)lung disease, (ii)Karnofsky Performance Rating Scale (KPS) and (iv) age Multidimensional frailty: (i) IADLs, (ii)physical function, (iii)comorbidities, (iv) number of daily medications, (v) vision, (vi)hearing, (vii)nutrition, (viii) mental health and (ix) social activity and (x)cognition.①The International Myeloma Working Group (IMWG) Frailty Index; ②the Revised Myeloma Comorbidity Index (R-MCI); and ③the Carolina Frailty Index (CFI)
Bréchemier et al. [ 31 ](2019)FranceCross-sectional ( n = 418)Any malignant tumorN/AMultidimensional frailty(i) nutrition, (ii) comorbidities, (iii)cognition, (iv) functional autonomy, (v) physical performanceCGA
Anusa et al. [ 32 ] (2019)IndiaCross-sectional( n = 520)Head and neck cancersN/AEmotional frailty(i) Poor correspondence, (ii)anxiety and (iii)depressionN/A
Zhang et al. [ 44 ] (2019)ChinaTheoretical Review (n/a)Any malignant tumorsFrailty is an unstable state of increased vulnerability to stressors and high risk of adverse health outcomes.Multidimensional frailtyN/AN/A
Zhang et al. [ 33 ] (2018)ChinaCross-sectional ( n = 185)Lung cancerFrailty is a dynamic process that can be transformed in response to an individual’s environment and state of stress, and older patients in the course of a disease are more prone to developing frailty syndromes, which in turn affect their disease prognosisPhysical frailty, psychological frailty, social frailty and environmental frailtyPhysical frailty: (i) physical performance Psychological frailty: (i) mood and (ii) emotion Social frailty: (i) social relations and (ii) social support Environmental frailty: (i) housing environment and (ii)community environmentCFAI
Abel et al. [ 45 ] (2018)AmericaTheoretical Review (n/a)Hematologic malignanciesFrailty is a vulnerable state that arises from “decreased reserves in multiple organ systems, which are initiated by disease, lack of activity, inadequate nutritional intake, stress, and/or the physiologic changes of aging.”Multidimensional frailtyN/AN/A
Martinez-Tapia et al. [ 41 ](2018)FranceProspective cohort ( n = 1136)Any malignant tumorsN/AMultidimensional frailty(i)age, (ii) functional status, (iii) comorbidity, (iv) cognition, (v) mood and (vi)nutritionG8
Loh et al. [ 46 ](2017)AmericaTheoretical Review (n/a)Any malignant tumorsFrailty is a geriatric syndrome conceptualized as decreased physiological reserve and functional status across multiple organ systems leading to increased vulnerability to stressors and adverse outcomes.Multidimensional frailty(i) functional status, (ii) comorbidities, (iii) psychological health, (iv) nutritional status, (v) social support, (vi)cognition, (vii)number of medications, and (viii)geriatric syndromes.CGA
Winters-Stone et al. [ 47 ](2015)AmericaTheoretical Review (n/a)Any malignant tumorsFrailty is an overall weakened physiological state and is usually associated with advanced age.Physical frailty(i) involuntary weight loss, (ii) reduced grip strength, (iii) fatigue, (iv) decline in physical activity, and (v) slow walking speed.FP
Baijal et al. [ 48 ] (2014)AmericaTheoretical Review (n/a)Any malignant tumorsPhysical frailty is defined as “a medical syndrome with multiple causes and contributors that is characterized by decreased strength and endurance and reduced physiologic function that can lead to dependency and death.Physical frailtyN/AFP; FI; CGA; FRAIL scale
Bugat et al. [ 49 ] (2014)FranceTheoretical Review (n/a)Any malignant tumorN/APhysical frailty(i) energy balance-nutrition, (ii) physical activity, (iii) nervous system, (iv) vascular system, (v) strength, (vi) endurance, and (vii) gait speedThe Frailty Trait Scale
Ponzetti et al. [ 42 ] (2014)ItalyProspective cohort ( n = 350)Any malignant tumorFrailty has been defined as a gradual, preventable process beginning after a period of inactivity, stress or inadequate nutrition, with progression to accelerating functional decline and increased risk of adverse events such as falls, disability, hospitalization, and deathPhysical frailty and Psychosocial frailtyPhysical frailty: (i) neoplastic invasion of the central nervous system (CNS), malignant hypercalcemia and recurrent serous effusion, (ii) Severe comorbid conditions, Charlson-Deyo score ≥ 5, (iii) Severe uncontrolled symptoms, (iv) Severe dependence in ADLs or IADLs, (v) More than two urgent hospitalizations in the previous 3 months. Psychosocial frailty: (i) lack of adequate social support evidenced: living alone; housing problems (no lift while living at high floor, no central heating, homeless); lack of an adequate care giver. (ii) Conditions indicating frail psychosocial conditions: communication barriers; clear and repeated requests for hastened death; clear family discord; unresolved or multiple prior losses repeatedly mentioned during the clinical interview; serious economic limitations; patient’s repeated concerns about the care of relatives. (iii) Evidence of a deep ongoing spiritual or existential crisis.Adapted from CGA

Definitions of multidimensional frailty

Of the 25 articles included, 19 defined multidimensional frailty or some dimension of frailty [ 25 – 30 , 33 – 35 , 37 , 38 , 40 , 42 – 48 ], but these definitions were not the same. It follows that there is no universally accepted way to identify or define frailty in the context of geriatric oncology. Although there is no clear consensus and definition of frailty, we have identified several key points of consensus in geriatric oncology regarding the concept of frailty by examining and synthesising from these definitions in the included studies: (i) Frailty is a condition of severely diminished functional reserve and increased vulnerability to stress, often leading to adverse health outcomes [ 25 – 30 , 33 – 35 , 37 , 38 , 40 , 42 – 48 ]. (ii) Cancer acts as a “catalyst” in the “frailty” process [ 25 , 29 , 33 , 37 , 43 , 47 ]. (iii) Frailty is a clinical syndrome that may be caused by age- and tumor-related mechanisms, including chronic inflammation, sarcopenia, comorbidities, and dysregulation of multiple physiological system [ 25 , 27 – 30 , 33 , 35 , 37 , 43 , 46 ]. (iv) Frailty is a dynamic, progressive, and preventable process whose central element is functional performance [ 25 , 29 , 30 , 33 – 35 , 42 , 43 , 47 , 48 ]. (v) The significance of frailty assessment is to help oncologists determine or adjust cancer treatment plans [ 25 – 27 , 30 , 35 , 37 , 38 , 40 , 42 – 46 , 48 ].

Dimensions of multidimensional frailty and the components under the corresponding dimensions

Physical frailty

Twenty articles in our scoping review addressed physical frailty [ 25 – 27 , 29 – 31 , 33 , 35 – 37 , 40 – 49 ], which is considered the most central dimension of frailty, and many scholars even equating frailty research with the study of physical frailty. Summarizing all the included articles involving physical frailty, we identified the following three sets of the most frequently used components of physical frailty (Table 1 ).

Physical performance and functional status are among the most frequently cited factors, including walking speed, grip strength, fatigue, balance (history of falls), activities of daily living (ADLs) and instrumental activities of daily living (IADLs). Most researchers consider physical performance and functional status to be core components of physical frailty [ 25 – 27 , 29 – 31 , 33 , 35 – 37 , 40 – 43 , 46 , 47 , 49 ].

Nutrition-related problems, including unintentional weight loss or decreased BMI are among the most frequently cited components of physical frailty in addition to physical performance and functional status [ 25 – 27 , 29 , 31 , 33 , 35 – 37 , 40 , 41 , 43 , 46 , 47 , 49 ].

Cancer type, hearing, vision, co-morbidity, polypharmacy were also highlighted as key components of physical frailty [ 25 , 29 , 31 , 33 , 36 , 37 , 40 – 43 , 46 , 49 ].

Psychological frailty

Of the articles we included, 14 papers referred to psychological frailty or emotional frailty, and by summarizing these articles [ 25 , 29 , 31 – 33 , 36 , 37 , 40 – 46 ], we identified the following three sets of the most commonly used components of psychological frailty (Table 1 ).

Mood problems, the most frequently mentioned component of psychological frailty, includes low moods such as tension, anxiety, depression, and sadness, and were the factors that researchers consider to be the most central to psychological frailty [ 25 , 29 , 33 , 36 , 37 , 41 ].

Emotion-related problems, such as loneliness, emptiness, and poor coping skills, were emotionally frailty and were another common component of psychological frailty [ 25 , 32 , 33 , 40 , 42 , 43 ].

Cognitive problems, including those related to low self-concept or poor self-assessed health, are somewhat controversial because of their similarity to cognitive frailty, but many researchers still believe that cognitive problems are also one of the common components of psychological frailty [ 29 , 31 , 36 , 37 , 40 , 41 , 43 , 46 ].

Social frailty

Summarizing all the 12 articles included that involved social frailty [ 25 , 29 , 33 , 34 , 36 – 40 , 42 , 43 , 46 ], we identified the following four sets of the most commonly used components of social frailty (Table 1 ).

Social roles or relationships, for example, are there people who can be relied upon and how many people are trusted and close? The patient’s role or relationship in society was considered to be one of the core components in measuring social frailty [ 25 , 33 , 38 , 39 , 43 ].

Social support, including subjective and objective support [ 29 , 33 , 34 , 36 – 39 , 42 , 46 ]. Subjective support is the patient’s emotional experience of being cared for, respected, and supported in society [ 50 ]. For example, the encouragement and emotional support of family and friends. Objective support is help that actually and specifically can help the patient [ 50 ]. For example, financial assistance, material resources, and improvement of living environment. Environmental frailty is defined as the inability of the residential home environment or community environment to meet the patient’s needs [ 51 ], which corresponds to the objective support situation, and therefore we consider it to be within the social frailty dimension. Social support was also one of the core components of what was considered to be social frailty.

Social activities, such as visiting friends, going out, and talking to someone, were also the main components of social frailty mentioned in most current studies [ 29 , 34 , 36 , 38 – 40 ].

Living alone, was also a key component of social frailty [ 29 , 34 , 36 , 38 , 39 , 42 ].

Cognitive frailty

Of the articles we included, 9 papers referred to cognitive frailty [ 25 – 27 , 31 , 37 , 40 , 41 , 43 , 46 ], and by summarizing these articles, we identified the following three sets of the most commonly used components of cognitive frailty (Table 1 ).

Memory impairment, such as complaining about one’s poor memory because of treatment strategies such as chemo-radiotherapy, memory impairment was considered by geriatric oncologists to be the most common component of cognitive frailty [ 25 – 27 ].

Attention deficit, also another common component of cognitive frailty [ 26 , 27 ].

Executive function, language, abstract thinking, numeracy, and orientation were also components that can be involved in cognitive frailty [ 26 , 31 , 37 ].

Oral frailty

Oral frailty was mentioned in one article included in this review [ 28 ], which conceptualized it as a distinct but emerging construct. Based on this article, we identified two sets of oral frailty components (Table 1 ).

Dental-related problems such as number of teeth, bite force of teeth, etc [ 28 ].

Subjective difficulty, including subjective difficulty in eating hard foods and swallowing [ 28 ].

Although only one included study explicitly examined oral frailty, our discussion group deemed it clinically and conceptually important to retain it as a separate dimension. This is because oral frailty has been increasingly recognized as an emerging construct in geriatric research, with clear links to nutrition, sarcopenia, and physical frailty [ 52 ], and it may serve as an early and modifiable indicator of multidimensional frailty. Thus, in some frameworks, oral frailty may be considered a subdomain or early indicator of physical frailty. A more comprehensive conceptual framework of multidimensional frailty can be ensured through the inclusion of oral frailty, while also reflecting the structure of the included literature, although we recognize its conceptual overlap with physical frailty.

Relationship between the dimensions of multidimensional frailty

Based on our scoping review, it was found that there is still ambiguity about the dimensions of frailty, some articles consider frailty to refer only to the physical frailty [ 30 , 35 , 47 – 49 ], and some articles consider frailty to be multidimensional, but they do not specify which dimensions are included in their multidimensional frailty [ 31 , 44 , 45 ]. Some articles define frailty as having three dimensions—physical, psychological, and social [ 29 , 36 ]; while others propose four dimensions, such as: physical, cognitive, emotional, and social [ 25 , 37 , 40 , 43 , 46 ]; or physical, psychological, social, and environmental [ 33 ]. Therefore, based on the included articles, we determined that the dimensions most routinely included in multidimensional frailty should be physical, psychological, social, and cognitive frailty, based on the frequency of dimensions in the literature as well as the discussions of our authors. Of these, physical frailty is the most central dimension and occurs most frequently in overall multidimensional frailty. Psychological frailty and social frailty come after physical frailty, but they both occur at a comparable frequency in overall multidimensional frailty. Further for cognitive frailty, it is less frequent in overall multidimensional frailty is more subordinate and has some association with psychological frailty, and oral frailty has the lowest frequency. In addition, we consider that emotional frailty can be contained within psychological frailty and environmental frailty can be contained within social frailty. The specific multidimensional frailty dimensions and and their corresponding content relations were shown in Fig. 2 .

Fig. 2 Multidimensional frailty dimensions and their corresponding content relations
Fig. 2 Multidimensional frailty dimensions and their corresponding content relations

Discussion

Definitions and dimensions of multidimensional frailty

Although a growing number of scholars in the field of geriatric oncology are aware of the importance of multidimensional frailty assessment, few have focused specifically on the concept of multidimensional frailty in the field. Using a scoping review approach, this study explored the concept of multidimensional frailty in the field of geriatric oncology, summarizing the dimensions of multidimensional frailty and the components under each dimension.

Based on the synthesis of included studies, we propose the following definition of multidimensional frailty in the context of geriatric oncology: Multidimensional frailty is a dynamic and potentially preventable clinical syndrome in which older adults with cancer experience a state of diminished functional reserve and increased vulnerability to internal and external stressors, including those related to aging, cancer progression, and cancer treatments [ 30 , 48 ]. It is characterized by functional decline or dysregulation across multiple domains, most centrally physical [ 35 ], but also psychological, social, cognitive [ 46 ], and in some cases, oral domain [ 28 ]. Cancer acts as a catalyst that may accelerate or aggravate frailty through mechanisms such as chronic inflammation, sarcopenia, multimorbidity, and polypharmacy [ 37 , 43 ]. Frailty can increase the risk of treatment-related complications, functional decline, and mortality [ 47 ]. Its recognition is therefore critical for oncologists to individualize care, estimate treatment tolerance, and adjust treatment planning appropriately [ 45 ]. The concepts and components of several existing dimensions of frailty were outlined and discussed in detail below.

Components of frailty under the corresponding dimensions

Physical frailty

Experts consider physical frailty to be an important medical syndrome with multiple etiological and causative factors, characterized by reduced physical strength, endurance and physiological functioning, which increases the likelihood of personal dependence and/or death [ 53 ]. Our review showed that indicators, such as step speed, grip strength, and ability to perform activities of daily living, were the most frequently cited components of physical frailty, probably due to the invasive and attritional nature of malignancy, coupled with the stressors of subsequent surgeries, radiotherapy, and other stressors, whereby patients suffer from a significant loss of muscle mass and quantity, predisposing them to impaired physical performance and functional status [ 54 ]. However, indicators such as step speed and grip strength need to be manipulated by professionals, and future work can be carried out to explore some simple and easy-to-access substitutable indicators.

Nutrition-related problems are another major core factor of physical frailty. Cancer patients often suffer from nutrition-related symptoms such as nausea and vomiting during the disease treatment process, resulting in malnutrition, cachexia and other adverse consequences [ 55 ], which in turn induce physical frailty [ 56 ]. Therefore, the nutritional status of oncology patients is an important indicator for assessing their physical frailty, and in the future, more accessible micro-nutritional indicators should be considered in addition to the common macro-indicators (weight, BMI).

In addition, there are indicators such as vision, hearing and co-morbidities, which are also commonly used to assess physical frailty, but the use of these indicators has not yet been standardized, and their use has been variable between studies. There is further scope for exploring more uniform components of physical frailty beyond physical functioning and nutrition in the future.

Psychological frailty

Psychological frailty is also an important dimension of frailty. Fitten described psychological frailty as brain alterations that are deviations from natural aging but are not necessarily diseases [ 57 ]. They contribute to decreased mood resilience when confronted with minor stressors and might induce adverse health results similar to physical frailty [ 57 ]. In the literature we included, there were no studies that examined psychological frailty in isolation; they were all considered in conjunction with other dimensions of frailty. This is in line with Shimada et al. who argue that psychological frailty must be considered alongside other dimensions of frailty (e.g., physical) [ 58 ] to fully define frailty. Furthermore, we consider emotional frailty to be included within the psychological frailty dimension.

Our results found that mood problems (tension, anxiety, depression, etc.) and emotional problems (loneliness, emptiness, etc.) were the most common core indicators of psychological frailty, and older adults with cancer often suffer from low mood and increased emotional demands due to their disease, which in turn causes a decline in psychological resilience and consequently psychological frailty [ 59 ]. In addition, cognitive problems in older adults with cancer were often recognized as one of the components of psychological frailty, but there is some controversy because they were also considered to be a major component of cognitive frailty [ 60 ]. After a review of the literature, we concluded that the cognitive problems of psychological frailty have some overlap with, but are not identical to, the components of cognitive frailty. Thus, cognitive frailty and psychological frailty are two different dimensions of frailty that exist at cross-purposes. Further research is needed to investigate the interactions between these two dimensions.

Social frailty

Recently, social frailty has gained recognition as a dimension of frailty, which is described as a continuum to assess the risk of losing social and general resources, activities, or abilities that are essential for fulfilling basic social needs over the course of an individual’s lifetime [ 61 ]. In this context, environmental frailty was defined as the difficulty of living in a family or community environment to meet the patient’s needs [ 51 ], which corresponds to a socially objective support situation, and therefore we included it in the social frailty dimension.

Social roles or relationships and social support are considered as determinants of social frailty [ 39 ]. Older adults with cancer, due to retirement as well as the diagnosis of the disease, are in a phase of role transition and adaptation, when they have a poorer sense of social belonging and are more likely to be frail, and studies have confirmed that patients with cancer with low social support are more likely to be frail than patients with cancer with high social support [ 39 ]. In addition, social activities such as visiting friends, going out, talking to someone, and the patients living alone are also common components in measuring social frailty [ 62 ]. Older adults with cancer may reject socialization because of the adverse physiological reactions to the disease itself, as well as the possible shame of the disease, resulting in social frailty, which later reduces socialization because of the frailty, creating a vicious cycle [ 39 ]. Because social frailty is modifiable, further research is needed to explore the impact of social interventions on survival in older adults with cancer.

Cognitive frailty

Recently, the concept of cognitive frailty has been proposed. There is growing support for cognitive frailty as a separate domain of frailty [ 63 ], but its definition is controversial. Some scholars have defined cognitive frailty as a bit of cognitive-related aspects of impairment resulting in frailty, while some studies have defined it as a heterogeneous clinical condition in which physical frailty coexists with mild cognitive impairment, but does not include other types of dementia such as Alzheimer’s disease [ 64 ]. Several studies have examined cognitive frailty in older adults and have shown that low cognitive functioning is significantly associated with the development of physical frailty, and that the interaction between the two exacerbates the development of cognitive frailty [ 65 ]. As for older population with cancer, in addition to cognitive impairment brought about by aging, tumors, radiotherapy, chemotherapy, and side effects of drugs may further aggravate cognitive impairment. However, since there are still few studies on cognitive frailty in older adults with cancer, and cognitive frailty is mostly measured based on cognitive components such as memory, attention, and executive ability [ 27 , 32 ], further investigation into the mechanisms of the onset and development of cognitive frailty in the field of oncology is needed in the future to expose the gold indexes that can truly assess cognitive frailty.

Oral frailty

Several studies have suggested that oral frailty is also an assessment dimension of frailty in older adults with cancer [ 28 ]. The Japanese Dental Association defines oral frailty as a set of phenomena in which poor oral health leads to low physical and mental functioning [ 66 ]. In terms of its connotation, it is mainly a patient’s oral-related problems, such as tooth loss and reduced chewing power, which lead to reduced direct nutritional intake and indirect self-image disorders resulting in depressed mood and reduced socialization [ 52 , 67 ]. The assessment of oral frailty in this study was mainly based on indicators such as the number of teeth, the occlusal force of the teeth, and the subjective degree of difficulty, but since this was only derived based on one piece of literature on oral frailty in older patients with cancer, the causes of oral frailty need to be further explored in the future in order to determine its final constituent elements.

Strengths and limitations of the study

The strength of this study lies in the systematic and comprehensive synthesis of concepts from the literature related to multidimensional frailty in the field of geriatric oncology, summarizing the dimensions that multidimensional frailty should encompass as well as the components under each dimension. Although this is only the first step in the conceptualization of multidimensional frailty in the field of geriatric oncology and the final results are preliminary, we believe that it is important for advancing the assessment as well as management of multidimensional frailty in the field of geriatric oncology. However, we acknowledge that our study also has some limitations. Firstly, we only included articles written in English and Chinese, suggesting that our findings may not cover all studies related to the concept of multidimensional frailty in the field of oncology. Secondly, the large number of different definitions of multidimensional frailty may mean we did not fully capture all of them in our proposed definition; however, key concepts that occurred repeatedly were included. Further work may be needed to reduce heterogeneity and uncertainty in the definitions used across studies.

Implications for future research

The results of our scoping review showed that the dimensions of multidimensional frailty in older adults with cancer mainly contain physical, psychological, social, cognitive, and oral, but the specific weighting ratio of each dimension on multidimensional frailty is still unclear. In the future, there is still a need to further explore the effects of deficiencies in different frailty dimensions on the multidimensional frailty of older adults with cancer, to clarify the specific weighting ratios of each dimension on the overall assessment of multidimensional frailty, and to determine what constitutes a validated tool for assessing frailty with a minimum number of dimensions to predict serious adverse events in older adults with cancer undergoing oncological treatment. In addition, we need to further identify the most representative components under each frailty dimension and explore the interactions between frailty components of different dimensions and the pathways through which negative interrelationships are formed to help us manage and prevent frailty more effectively.

Conclusion

This study comprehensively summarized the concept of multidimensional frailty in the field of geriatric oncology through a scoping review, and found that multidimensional frailty was a syndrome that centered on physical dimension, but also encompassing, psychological, social, cognitive, and oral dimensions, and that each of these dimensions of frailty has its own individual components. It is further proposed that an effective frailty assessment tool with a minimum number of dimensions can be constructed to predict serious adverse events for older adults with cancer in the future, as well as exploring the interactions and pathways between different dimensions, which is of great significance for the prevention and management of frailty in older adults with cancer, as well as for oncology rehabilitation.

Supplementary Information

Supplementary Material 1.

Acknowledgements

Not applicable.

Abbreviations

Activities of Daily Living

Instrumental activities of daily living

Charlson comorbidity Index

Groningen Frailty Indicator

Frailty phenotype

Montreal cognitive assessment

European Organization for Research and Treatment of Cancer Quality of Life Questionnaire

Geriatric assessment

Comprehensive geriatric assessment

Comprehensive Frailty Assessment Instrument

Geriatric 8

Frailty Index

Authors’ contributions

Study concept and design: Yinning Guo, Qin Xu, Lingyu Ding; Acquisition of data: Yinning Guo, Yimeng Chen; Analysis and interpretation of data: Yinning Guo, Yimeng Chen, Lingyu Ding, Shulin Song1, Ziyan Wang1, Yue Chen1; Drafting of the manuscript: Yinning Guo; Critical revision of the manuscript for important intellectual content: Qin Xu, Lingyu Ding, Zhongmin Fu.

Funding

This study was supported by project “The exploration of trajectories and intervention program of frailty for gastric cancer survivors based on the health ecology theory” supported by the National Natural Science Foundation of China (NSFC) (No.82073407), Project“Research on the dynamic interaction mechanism and collaborative intervention strategies of multiple frailty subtypes in elderly cancer survivors”supported by NSFC (No: 72404140), Project of “Nursing Science”Funded by the 4th Priority Discipline Development Program of Jiangsu Higher Education Institutions(Jiangsu Education Department(2023)No.11) and Project“Research on the mechanisms and intervention strategies of dietary behaviors of older gastric cancer survivors on frailty development under multi-temporal-situational interactions”supported by Jiangsu Province Postgraduate Scientific Research Innovation Program(KYCX25_2198).

Data availability

Not applicable.

Declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Footnotes

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Qin Xu, Email: qinxu@njmu.edu.cn.

Lingyu Ding, Email: lingyuding@163.com.

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Associated Data

Supplementary Materials

Supplementary Material 1.

Data Availability Statement

Not applicable.

ИП Урсолов Владлен Сергеевич

ИНН 500118482352 · ОГРНИП 314500117700049

Реквизиты и контакты