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Barriers to palliative and hospice care utilization in older adults with cancer: A systematic review

Published:November 04, 2019DOI:https://doi.org/10.1016/j.jgo.2019.09.017

      Abstract

      The number of older adults with cancer and the need for palliative care among this population is increasing in the United States. The objective of this systematic review was to synthesize the evidence on the barriers to palliative and hospice care utilization in older adults with cancer. A systematic literature search was conducted using PubMed, CINAHL, PsycINFO, Embase, and Cochrane Library databases (from inception to 2018) in accordance to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. Research articles that examined palliative or hospice care utilization in older adults with cancer were included in this review. Fineout-Overholt's Level of Evidence was used for quality appraisal. A total of 19 studies were synthesized in this review. Barriers to palliative and hospice care utilization were categorized into socio-demographic barriers, provider-related barriers, and health insurance-related barriers. Findings revealed that male, racial minority, unmarried individuals, individuals with low socio-economic status or residing in rural areas, and fee-for-service enrollees were less likely to use palliative or hospice care. Lack of communication with care providers is also a barrier of using palliative or hospice care. The factors identified in this review provide guidance on identification of high-risk population and intervention development to facilitate the use of palliative and hospice care in older adults with cancer. Larger prospective studies on this topic are needed to address this critical issue.

      Keywords

      1. Introduction

      Cancer is the second leading cause of death in the United States, after heart disease affecting over 15.5 million individuals []. Older age is one of the most common risk factors for development of cancer []. The incidence of cancer is the highest among older adults in the United States. Approximately 60% of cancers in the United States occur in people aged 65 and older [
      • Cancer.Net
      Aging and cancer.
      ]. Older adults with cancer have high symptom burden and exhibit multiple physical and psychological symptoms including nausea/vomiting, fatigue, loss of appetite, weight loss, altered sleep, musculoskeletal symptoms, neurocognitive symptoms, urinary symptoms, circulatory symptoms, and hormonal symptoms [
      • Gift AG
      • Jablonski A
      • Stommel M
      • Given CW
      Symptom clusters in elderly patients with lung cancer.
      ,
      • Roinald RA
      • Heidrich SM
      Symptom clusters and quality of life in older breast cancer survivors.
      ]. These symptoms significantly affect the quality of life of older adults with cancer [
      • Roinald RA
      • Heidrich SM
      Symptom clusters and quality of life in older breast cancer survivors.
      ]. Older adults with cancer also have unique health needs not just associated with the disease itself but also due to bio-psycho-social changes caused due to the aging process as well [
      • Yates P
      • Miaskowski C
      • Cataldo JK
      • Paul SM
      • Cooper BA
      • Alexander K
      • et al.
      Differences in composition of symptom clusters between older and younger oncology patients.
      ]. Older adults with cancer have high levels of unmet needs including psychological needs, informational needs, and communication needs [
      • Puts MT
      • Papoutsis A
      • Springall E
      • Tourangeau AE
      A systematic review of unmet needs of newly diagnosed older cancer patients undergoing active cancer treatment.
      ,
      • van Weert JC
      • Bolle S
      • van Dulmen S
      • Jansen J
      Older cancer patients’ information and communication needs: what they want is what they get?.
      ].
      Older adults with cancer can benefit from early enrollment in palliative care services. Early utilization of palliative care is associated with symptom relief, improved mood, reduced depressive symptoms, improved quality of life and survival, overall satisfaction with treatment outcomes, and reduced cost of care [[
      • Bakitas MA
      • Tosteson TD
      • Li Z
      • Lyons KD
      • Hull JG
      • Li Z
      • et al.
      Early versus delayed initiation of concurrent palliative oncology care: patient outcomes in the ENABLE III randomized controlled trial.
      ,
      • Bauman JR
      • Temel JS
      The integration of early palliative care with oncology care: the time has come for a new tradition.
      ,
      • Greer JA
      • Pirl WF
      • Jackson VA
      • Muzikansky A
      • Lennes IT
      • Heist RS
      • et al.
      Effect of early palliative care on chemotherapy use and end-of-life care in patients with metastatic non–small-cell lung cancer.
      ,
      • Irwin KE
      • Greer JA
      • Khatib J
      • Temel JS
      • Pirl WF
      Early palliative care and metastatic non-small cell lung cancer: potential mechanisms of prolonged survival.
      ,
      • Temel JS
      • Greer JA
      • El-Jawahri A
      • Pirl WF
      • Park ER
      • Jackson VA
      • et al.
      Effects of early integrated palliative care in patients with lung and GI cancer: a randomized clinical trial.
      ,
      • Dalal S
      • Bruera E
      End-of-life care matters: palliative cancer care results in better care and lower costs.
      ]]. Despite the scientific evidence of the benefits associated with palliative care services, there are several barriers to palliative care utilization in older patients with cancer and older adults utilize palliative care services to a lesser extent compared to their younger counterparts [
      • Burge FI
      • Lawson BJ
      • Johnston GM
      • Grunfeld E
      A population-based study of age inequalities in access to palliative care among cancer patients.
      ,
      • Hui D
      • Kim SH
      • Kwon JH
      • Tanco KC
      • Zhang T
      • Kang JH
      • et al.
      Access to palliative care among patients treated at a comprehensive cancer center.
      ].
      Similarly, older adults with cancer can benefit from hospice care services. Hospice care helps address the multidimensional needs of the patients and families and provides support to patients' family during the illness and following death [
      • Ornstein KA
      • Aldridge MD
      • Mair CA
      • Gorges R
      • Siu AL
      • Kelley AS
      Spousal characteristics and older adults’ hospice use: understanding disparities in end-of-life care.
      ] and is associated with improved quality of life of patients near the end of their lives [
      • Wright AA
      • Keating NL
      • Balboni TA
      • Matulonis UA
      • Block SD
      • Prigerson HG
      Place of death: correlations with quality of life of patients with cancer and predictors of bereaved caregivers’ mental health.
      ]. Hospice care also improves family functioning, provides bereavement support [
      • Abernethy AP
      • Currow DC
      • Fazekas BS
      • Luszcz MA
      • Wheeler JL
      • Kuchibhatla M
      Specialized palliative care services are associated with improved short-and long-term caregiver outcomes.
      ], and increases patient satisfaction with care [
      • Teno JM
      • Mor V
      • Ward N
      • Roy J
      • Clarridge B
      • Wennberg JE
      • et al.
      Bereaved family member perceptions of quality of end-of-life care in US regions with high and low usage of intensive care unit care.
      ]. Enrollment in hospice also reduces overall Medicare costs [
      • Kelley AS
      • Deb P
      • Du Q
      • Aldridge Carlson MD
      • Morrison RS
      Hospice enrollment saves money for Medicare and improves care quality across a number of different lengths-of-stay.
      ]. However, evidence suggests only half of the patients who die of cancer are ever referred to hospice [
      • Von Gunten CF
      • Lutz S
      • Ferris FD
      Why oncologists should refer patients earlier for hospice care.
      ]. In most cases, patients with cancer are not referred to hospice until they approach very end of their life with only a few days to live. As a result, the patients and families are unable to fully benefit from the holistic approach to care [
      • Wittenberg-Lyles EM
      • Sanchez-Reilly S
      Palliative care for elderly patients with advanced cancer: a long-term intervention for end-of-life care.
      ]. One of the primary reasons for the lack of or low enrollment for hospice services is a lack of awareness of the benefits of hospice care. Patients and families are mostly informed about the philosophy of hospice care but are not informed about the practical benefits of hospice care, who provides the care, and how it is provided [
      • Casarett D
      • Crowley R
      • Stevenson C
      • Xie S
      • Teno J
      Making difficult decisions about hospice enrollment: what do patients and families want to know?.
      ]. Moreover, provider's discomfort with end-of-life issues discussions or time constraints in clinical settings were noted as some of the barriers to a timely referral of hospice service [
      • Von Gunten CF
      Discussing hospice care.
      ].
      The rapid growth in the number of older adults with the diagnosis of cancer accentuates the importance of gaining a better understanding of barriers to palliative or hospice care utilization among older adults with cancer. Yet, evidence on the use of palliative and hospice care in older adults with cancer has not been systematically reviewed. Therefore, the goal of this systematic review was to synthesize the scientific evidence on barriers to utilization of palliative and hospice care among older patients with cancer.

      2. Methods

      2.1 Literature search and selection

      Comprehensive literature searches were conducted using the PubMed, Cumulative Index of Nursing and Allied Health Literature (CINAHL), PsycINFO, Embase, and Cochrane Library databases. The key words for literature search included (cancer OR neoplasms OR oncology) AND (“palliative care” OR “supportive care” OR “end of life” OR hospice OR terminal OR dying) AND (barriers OR obstacles OR challenges OR difficulties) from inception to June 2018. Articles were limited by age filter of ‘aged 65 and above’ to focus on articles related to older adults. Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines were followed for literature search [
      • Moher D
      • Liberati A
      • Tetzlaff J
      • Altman DG
      • Prisma Group
      Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.
      ]. Ancestry searches were conducted from identified studies and manual search was conducted to retrieve additional research articles.
      This systematic review included articles that examined either palliative or hospice care utilization in older adults with cancer. For the purpose of this review, older adults are defined as individuals of age of 65 or older. Articles were included if they met the following inclusion criteria: 1) focused on older adults with cancer, 2) examined the factors associated with palliative or hospice care utilization, 3) published in a peer-reviewed journal, 4) written in English language, and 5) have accessible full text. To be broad and inclusive, for articles that include participants across age groups, articles were included as long as they reported on the older age group. This review only included original research, but no restrictions were placed on research design in order to maximize all relevant research evidence available on this topic. Quantitative, qualitative or mixed methods studies were deemed eligible for inclusion in this study. Systematic review studies were not used in this analysis; instead, they were used to identify relevant articles. Using this approach, the current systematic review aimed to comprehensively explore the barriers to palliative and hospice care utilization among older adults with cancer. Studies were excluded if they 1) focused on diseases other than cancer, 2) did not focus on older adults 3) did not address factors associated with palliative or hospice care utilization 4) editorial, commentaries, case studies, or research protocols.

      2.2 Data extraction

      The article selection process is depicted in Fig. 1. Two researchers (J.P. and A.T.) independently reviewed the titles and abstracts of each article to determine eligibility. The full texts of potentially eligible articles were retrieved for further review. Two researchers (J.P and A. T.) independently screened full texts of all potential articles and determined the eligibility of each article through discussion and consensus. In cases of discrepancy, the two researchers reconciled the decision and a third researcher (Y. J. or J. H.) was consulted as needed until the agreement was reached. The article selection process yielded a total of 19 final articles.
      Data from the 19 eligible articles were extracted independently by two researchers (J.P., A.T.). Data extracted included authors, the country where the study was conducted, sample, predictors/participant characteristics, outcome measures, and results. A standardized data extraction form was used for data extraction. Researchers met to discuss and resolve any discrepancies in data extraction.

      2.3 Quality appraisal

      The quality of included studies was assessed using Fineout-Overholt's Level of Evidence [
      • Fineout-Overholt E
      • Melnyk BM
      • Stillwell SB
      • Williamson KM
      Evidence-based practice step by step: critical appraisal of the evidence: part I.
      ]. Two reviewers (J.P and A.T.) evaluated the level of evidence of each article independently and any disagreements were brought to the group to reach a consensus.

      3. Results

      The study selection process is illustrated in Fig. 1. The initial search yielded 1958 articles in total from all five databases. Of these, 213 duplicate articles were excluded. Of the remaining 1745 articles, 1602 articles were excluded based on the review of the title and abstract. The full text of the remaining 143 articles and 9 articles identified through ancestry and search (n = 152) were reviewed. A total of 19 studies met the inclusion criteria and were included in the final sample of this study. Of the 19 studies identified, 14 studies examined hospice care utilization, four studies examined palliative care utilization, while one study examined both. The characteristics of each study are presented in detail Table 1.
      Table 1Description of studies included.
      Article/countryStudy designSamplePredictorsType of serviceResults
      Burge et al., (2008)

      Canada
      Retrospective population-based study (Secondary analysis of linked individual level information)7511 patients who died with cancer between 1998 and 2003Age, gender, race, SES, geographic residencePalliative careOlder subjects were significantly less likely than those <65 years of age to be registered with a PCP, particularly those aged 85 years and older (adjusted OR: 0.4; 95% CI: 0.3–0.5)
      Gani et al., (2018)

      United States
      Retrospective cross-sectional analysis (data from NIS)282,899 patients were identified who met the inclusion criteriaAge, race, health insurancePalliative careAmong all patients, 8.5% received a PC consultation during their admission. Patient age (age ≥ 75 years: OR = 2.54) was associated with greater odds of receiving PC (p < 0.05) and a member of a racial minority (27.6% vs. 30.2%, p < 0.001). Individuals with Medicare were more likely to receive PC (53.8%, p < 0.0001)
      Gidwani et al., (2016)

      United States
      Retrospective analysis (administrative data for veterans aged 65 years or older)11,896 veterans aged 65 years or older with cancer who died in 2012Health insurance, type of cancerPalliative and hospice careMost veterans (71%) received hospice care, whereas only 52% received palliative care. Patients with VA hospice care significantly less likely to receive hospice care for at least three days compared to those who received VA-Purchased or Medicare hospice care
      Hardy et al., (2011)

      United States
      Retrospective analysis (SEER Medicare database)117,894 individuals aged 66 and older with non-small cell lung cancer (NSCLC) who received hospice services in the last 6 months and died between 1991 and 2005Race, SESHospice careIn urban area blacks (OR = 0.79; 95% CI = 0.63–0.82), Asian/Pacific Islanders (OR = 0.42; 95% CI = 0.39–0.46) and Hispanics (OR = 0.81; 95% CI = 0.73–0.91) were less likely to receive hospice services compared to whites. In rural areas blacks were 21% less likely to received hospice services (0.79; 95% CI = 0.63–0.98). Patients in lowest SES quartile were 7% less likely to receive hospice services (OR = 0.93, 95% CI = 0.86–1.00)
      Kumar et al., (2012)

      United States
      Cross-sectional313 patients with a primary diagnosis of cancer seen in 3 outpatient oncology clinics at one academic cancer centerAge, race, marital status, SESPalliative care50% of the participants had not used palliative and supportive care services
      Miesfeldt et al., (2012)

      United States
      Retrospective analysis (Medicare claims data)235,821 Medicare parts A and B, fee-for-service patients dying with poor prognosis cancerAge, gender, raceHospice careOlder age (OR = 0.92; 95% CI 0.89–0.95), female gender (OR = 0.84; 95% CI 0.81–0.86) and black race (OR 0.81, 95% CI 0.76–0.86) was associated with late hospice enrollment
      McCarthy et al., (2003)

      United States
      Retrospective analysis (SEER Medicare database)62,117 patients with the diagnosis of lung or colorectal cancerAge, gender, race, marital status, SES, geographic residence, health insuranceHospice care20% entered hospice within 1 week of death, 6% entered >6 months before death. Factors with later hospice enrollment: being male, non-white, non-black race, having fee for service insurance, residing in a rural community. Also associated with shorter stays in hospice
      Lackan et al., (2003)

      United States
      Retrospective analysis (SEER Medicare database)25,161 female, aged 65 and older, living in one of SEER areas, diagnosed with breast cancerAge, race, marital status, SES, geographic residenceHospice care20.7% used hospice care before they died. Inverse relationship between use of hospice and age (p < 0.001). Higher use among married patients (p < 0.001). No differences in use by ethnicity. Significant differences in hospice usage based on geographic residence, income and educational level (p < 0.001)
      Lackan et al., (2004)

      United States
      Retrospective analysis (SEER Medicare database)170,136 individuals aged 67 and older diagnosed with breast, colorectal, lung, or prostate cancer from 1991 to 1996 and who died between 1991 and 1999Age, gender, race, marital status, SES, geographic residence, health insuranceHospice careThe rate of hospice utilization was higher for subjects who were younger, married, female, non-Hispanic white, living in urban areas, diagnosed with lung or colorectal cancer, and living in areas with higher income and education levels
      Lackan et al., (2005)

      United States
      Retrospective analysis (SEER Medicare database)71,948 patients diagnosed with breast, colorectal, lung or prostate cancer from 1991 to 1996, and died between 1991 and 1999Gender, marital status, geographic residenceHospice careCurrently married (OR = 1.36, 95% CI = 1.28–1.45) or ever married (OR = 1.23, 95% CI = 1.16–1.31) subjects were more likely to use hospice than never married subjects. A significant interaction between marital status and gender (p < 0.001) was observed
      Nayar et al., (2014)

      United States
      Retrospective analysis (SEER Medicare database)91,039 Medicare beneficiaries who died in 2008Age, gender, race, SES, geographic residenceHospice careRacial minority were less likely to have ever used hospice or be enrolled in hospice in last 3 days of life compared on non-Hispanic Whites. In addition, patients with low SES were less likely to ever use hospice or be enrolled in hospice care within last 3 days compared to patients with high SES
      Ngo-Metzger, (2003)

      United States
      Retrospective analysis (SEER Medicare database)184,081 patients who died of primary lung, colorectal, prostrate, breast, gastric, or liver cancer between 1988 and 1998Race, geographic residenceHospice careAfter adjustment, patients who were Asian American (OR = 0.67; 95% CI = 0.62 to 0.73) and born abroad (OR = 0.90; 95% CI = 0.86 to 0.94) were less likely to use hospice care than were white patients
      Noordman et al., (2017)

      Netherlands
      Mixed methods (quantitative secondary data analysis and qualitative interviews)Patients with the diagnosis of cancer (n = 126) of which 70 were aged 65 and older and 56 were younger patients (aged 18–65)Supportive care interventionsBarriers and facilitator related to attributes of themselves (impact of dx, feeling modest or shy, uncomfortable with provider especially intimate issues, forgetting questions self-efficacy, feeling sick), provider (taking patient seriously, not feeling connected, topics or emotions not being discussed, lack of information) and healthcare system (time restriction, inefficient communication between different providers)
      Saito et al., (2011)

      United States
      Retrospective analysis (SEER Medicare database)7879 patients aged 65 and older who died of lung cancer from 1991 through 1999Age, gender, race, geographic residence, SESHospice careBeing older, female, non-Hispanic white, residing in urban areas and higher SES were associated with hospice use
      Sharma et al., (2016)

      United States
      Retrospective analysis (chart review)567 veterans who died with advanced cancer between 2002 and 2009Age, race, marital status, type/location of cancerHospice careOlder adults had earlier referral to hospice care (mean DOR: 47.3, p = 0.015), and longer stay with hospice (mean LoS: 32.5, p = 0.007)
      Shugarman et al., (2008)

      United States
      Retrospective cohort study13,120 medicare decedents with lung cancerAge, genderHospice careWomen were more likely to use hospice services (14% more likely than men). Older cohorts were significantly more likely to have used hospice services in their last years of life
      Smith et al., (2009)

      United States
      Retrospective analysis (SEER Medicare database)40,960 fee-for-service (FSS) Medicare beneficiaries aged 65 and older with advanced cancerRaceHospice careCompared to Whites (42%), hospice enrollment was lower for black (36.9%), Asian (32.2%), and Hispanic (37.7%) patients
      Tromantano et al., (2018)

      United States
      Retrospective analysis (SEER Medicare database)6449 patients with cancer of which 3597 (55.8%) enrolled in hospiceAge, gender, race, SES, geographic residenceHospice careAmong hospice-enrolled patients, 31.4% enrolled in the last 7 days of life. Patients who were older, female, with stage IV disease, or those with higher socioeconomic status were more likely to enroll in hospice
      Watanabe-Galloway et al., (2016)

      United States
      Retrospective analysis (medicare claims data)34,975 beneficiaries with colorectal cancer who died in 2008Geographic residence, race, SESHospice careBeneficiaries in rural counties were less likely to ever use hospice (OR = 0.78) compared to those in metropolitan counties after adjusting for demographic factors. Beneficiaries from racial/ethnic minority groups and lower SES were less likely to ever use hospice
      Note: CI: confidence interval; OR: odds ratio: PCP: primacy care provider; NIS: ational npatient ample; SEER: urveillance, pidemiology, and nd esults; SES: socio-economic status.

      3.1 Study description and level of evidence

      The majority of studies were retrospective analysis that identified different demographic and contextual barriers associated with palliative/hospice care utilization. Among the 19 studies identified, 18 studies were quantitative, and one study was a mixed methods design. Among the 18 quantitative studies, 17 had retrospective designs using secondary data analysis while one study had a cross-sectional design. The mixed methods study was a combination of retrospective quantitative analysis and qualitative study. The quality of identified studies was rated on a 7-point scale using Fineout-Overholt's hierarchy of evidence [
      • Fineout-Overholt E
      • Melnyk BM
      • Stillwell SB
      • Williamson KM
      Evidence-based practice step by step: critical appraisal of the evidence: part I.
      ] based on the study design (level 1 represented the highest level and level 7 represented the lowest level).

      3.2 Sample characteristics

      Study population included older adults with cancer in all studies. The sample sizes of the studies ranged from 70 participants to 282,899 participants. The majority of the studies (n = 17, 89%) were conducted in the U.S., one study was conducted in Canada, and one study was conducted in the Netherlands. The major predictors of hospice/palliative care use were age, gender, race, marital status, socio-economic status, geographic residence, and health insurance. The age of the participants included were 65 and older, race of the participants examined included Caucasian/Non-Hispanic White, African American/Non-Hispanic Black, Asian, Hispanic, and Pacific Islanders. The studies examined various types of cancer, including lung cancer, breast cancer, GI cancer, colorectal cancer, prostate cancer, hematologic cancer, pancreatic cancer, liver cancer, esophageal cancer, and other cancers.

      3.3 Types of services examined

      The types of services examined were either hospice care or palliative care. Four studies examined palliative care [
      • Burge FI
      • Lawson BJ
      • Johnston GM
      • Grunfeld E
      A population-based study of age inequalities in access to palliative care among cancer patients.
      ,
      • Kumar P
      • Casarett D
      • Corcoran A
      • Desai K
      • Li Q
      • Chen J
      • et al.
      Utilization of supportive and palliative care services among oncology outpatients at one academic cancer center: determinants of use and barriers to access.
      ,
      • Noordman J
      • Driesenaar JA
      • Henselmans I
      • Verboom J
      • Heijmans M
      • van Dulmen S
      Patient participation during oncological encounters: barriers and need for supportive interventions experienced by elderly cancer patients.
      ,
      • Gani F
      • Enumah ZO
      • Conca-Cheng AM
      • Canner JK
      • Johnston FM
      Palliative care utilization among patients admitted for gastrointestinal and thoracic cancers.
      ], one study examined both palliative and hospice care [
      • Gidwani R
      • Joyce N
      • Kinosian B
      • Faricy-Anderson K
      • Levy C
      • Miller SC
      • et al.
      Gap between recommendations and practice of palliative care and hospice in cancer patients.
      ], while the remaining fourteen studies examined hospice care utilization.

      3.4 Study findings on barriers to palliative/hospice care utilization

      The predictors examined by the studies included age, gender, race/ethnicity, marital status, socio-economic status, geographic residence, provider factors, and health insurance. In this review, the results are sorted into three categories: 1) socio-demographic barriers, 2) provider-related barriers, and 3) health-insurance related barriers.

      3.4.1 Socio-demographic barriers

      Seventeen of the nineteen studies reported results on the association of socio-demographic factors to palliative or hospice care utilization [
      • Burge FI
      • Lawson BJ
      • Johnston GM
      • Grunfeld E
      A population-based study of age inequalities in access to palliative care among cancer patients.
      ,
      • Kumar P
      • Casarett D
      • Corcoran A
      • Desai K
      • Li Q
      • Chen J
      • et al.
      Utilization of supportive and palliative care services among oncology outpatients at one academic cancer center: determinants of use and barriers to access.
      ,
      • Hardy D
      • Chan W
      • Liu CC
      • Cormier JN
      • Xia R
      • Bruera E
      • et al.
      Racial disparities in the use of hospice services according to geographic residence and socioeconomic status in an elderly cohort with nonsmall cell lung cancer.
      ,
      • Lackan NA
      • Freeman JL
      • Goodwin JS
      Hospice use by older women dying with breast cancer between 1991 and 1996.
      ,
      • Ngo-Metzger Q
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Li FP
      • Phillips RS
      Older Asian Americans and Pacific Islanders dying of cancer use hospice less frequently than older white patients.
      ,
      • Lackan NA
      • Ostir GV
      • Freeman JL
      • Mahnken JD
      • Goodwin JS
      Decreasing variation in the use of hospice among older adults with breast, colorectal, lung, and prostate cancer.
      ,
      • Lackan NA
      • Ostir GV
      • Kuo YF
      • Freeman JL
      The association of marital status and hospice use in the USA.
      ,
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Phillips RS
      Barriers to hospice care among older patients dying with lung and colorectal cancer.
      ,
      • Miesfeldt S
      • Murray K
      • Lucas L
      • Chang CH
      • Goodman D
      • Morden NE
      Association of age, gender, and race with intensity of end-of-life care for medicare beneficiaries with cancer.
      ,
      • Nayar P
      • Qiu F
      • Watanabe-Galloway S
      • Boilesen E
      • Wang H
      • Lander L
      • et al.
      Disparities in end of life care for elderly lung cancer patients.
      ,
      • Smith AK
      • Earle CC
      • McCarthy EP
      Racial and ethnic differences in end-of-life care in fee-for-service medicare beneficiaries with advanced cancer.
      ,
      • Tramontano AC
      • Nipp R
      • Kong CY
      • Yerramilli D
      • Gainor JF
      • Hur C
      Hospice use and end-of-life care among older patients with esophageal cancer.
      ,
      • Gani F
      • Enumah ZO
      • Conca-Cheng AM
      • Canner JK
      • Johnston FM
      Palliative care utilization among patients admitted for gastrointestinal and thoracic cancers.
      ,
      • Watanabe-Galloway S
      • Zhang W
      • Watkins K
      • Islam KM
      • Nayar P
      • Boilesen E
      • et al.
      Quality of end-of-life care among rural medicare beneficiaries with colorectal cancer.
      ,
      • Saito AM
      • Landrum MB
      • Neville BA
      • Ayanian JZ
      • Weeks JC
      • Earle CC
      Hospice care and survival among elderly patients with lung cancer.
      ,
      • Shugarman LR
      • Bird CE
      • Schuster CR
      • Lynn J
      Age and gender differences in medicare expenditures and service utilization at the end of life for lung cancer decedents.
      ,
      • Sharma N
      • Sharma AM
      • Wojtowycz MA
      • Wang D
      • Gajra A
      Utilization of palliative care and acute care services in older adults with advanced cancer.
      ]. The socio-demographic factors examined included age, gender, race, marital status, socio-economic status (SES), and geographic residence. The association of each factor with palliative or hospice care utilization is discussed individually below.

      3.4.1.1 Age

      Twelve studies evaluated age as a correlate [
      • Burge FI
      • Lawson BJ
      • Johnston GM
      • Grunfeld E
      A population-based study of age inequalities in access to palliative care among cancer patients.
      ,
      • Kumar P
      • Casarett D
      • Corcoran A
      • Desai K
      • Li Q
      • Chen J
      • et al.
      Utilization of supportive and palliative care services among oncology outpatients at one academic cancer center: determinants of use and barriers to access.
      ,
      • Lackan NA
      • Freeman JL
      • Goodwin JS
      Hospice use by older women dying with breast cancer between 1991 and 1996.
      ,
      • Lackan NA
      • Ostir GV
      • Freeman JL
      • Mahnken JD
      • Goodwin JS
      Decreasing variation in the use of hospice among older adults with breast, colorectal, lung, and prostate cancer.
      ,
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Phillips RS
      Barriers to hospice care among older patients dying with lung and colorectal cancer.
      ,
      • Miesfeldt S
      • Murray K
      • Lucas L
      • Chang CH
      • Goodman D
      • Morden NE
      Association of age, gender, and race with intensity of end-of-life care for medicare beneficiaries with cancer.
      ,
      • Nayar P
      • Qiu F
      • Watanabe-Galloway S
      • Boilesen E
      • Wang H
      • Lander L
      • et al.
      Disparities in end of life care for elderly lung cancer patients.
      ,
      • Tramontano AC
      • Nipp R
      • Kong CY
      • Yerramilli D
      • Gainor JF
      • Hur C
      Hospice use and end-of-life care among older patients with esophageal cancer.
      ,
      • Gani F
      • Enumah ZO
      • Conca-Cheng AM
      • Canner JK
      • Johnston FM
      Palliative care utilization among patients admitted for gastrointestinal and thoracic cancers.
      ,
      • Saito AM
      • Landrum MB
      • Neville BA
      • Ayanian JZ
      • Weeks JC
      • Earle CC
      Hospice care and survival among elderly patients with lung cancer.
      ,
      • Shugarman LR
      • Bird CE
      • Schuster CR
      • Lynn J
      Age and gender differences in medicare expenditures and service utilization at the end of life for lung cancer decedents.
      ,
      • Sharma N
      • Sharma AM
      • Wojtowycz MA
      • Wang D
      • Gajra A
      Utilization of palliative care and acute care services in older adults with advanced cancer.
      ]. Six studies found that an advanced age served as a barrier to palliative or hospice care enrollment, and older adults were less likely to use palliative/hospice care compared to the younger counterparts [
      • Burge FI
      • Lawson BJ
      • Johnston GM
      • Grunfeld E
      A population-based study of age inequalities in access to palliative care among cancer patients.
      ,
      • Kumar P
      • Casarett D
      • Corcoran A
      • Desai K
      • Li Q
      • Chen J
      • et al.
      Utilization of supportive and palliative care services among oncology outpatients at one academic cancer center: determinants of use and barriers to access.
      ,
      • Lackan NA
      • Freeman JL
      • Goodwin JS
      Hospice use by older women dying with breast cancer between 1991 and 1996.
      ,
      • Lackan NA
      • Ostir GV
      • Freeman JL
      • Mahnken JD
      • Goodwin JS
      Decreasing variation in the use of hospice among older adults with breast, colorectal, lung, and prostate cancer.
      ,
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Phillips RS
      Barriers to hospice care among older patients dying with lung and colorectal cancer.
      ,
      • Miesfeldt S
      • Murray K
      • Lucas L
      • Chang CH
      • Goodman D
      • Morden NE
      Association of age, gender, and race with intensity of end-of-life care for medicare beneficiaries with cancer.
      ]. In contrast, six studies found that older patients with cancer were more likely to use palliative/hospice care services than younger patients [
      • Nayar P
      • Qiu F
      • Watanabe-Galloway S
      • Boilesen E
      • Wang H
      • Lander L
      • et al.
      Disparities in end of life care for elderly lung cancer patients.
      ,
      • Tramontano AC
      • Nipp R
      • Kong CY
      • Yerramilli D
      • Gainor JF
      • Hur C
      Hospice use and end-of-life care among older patients with esophageal cancer.
      ,
      • Gani F
      • Enumah ZO
      • Conca-Cheng AM
      • Canner JK
      • Johnston FM
      Palliative care utilization among patients admitted for gastrointestinal and thoracic cancers.
      ,
      • Saito AM
      • Landrum MB
      • Neville BA
      • Ayanian JZ
      • Weeks JC
      • Earle CC
      Hospice care and survival among elderly patients with lung cancer.
      ,
      • Shugarman LR
      • Bird CE
      • Schuster CR
      • Lynn J
      Age and gender differences in medicare expenditures and service utilization at the end of life for lung cancer decedents.
      ,
      • Sharma N
      • Sharma AM
      • Wojtowycz MA
      • Wang D
      • Gajra A
      Utilization of palliative care and acute care services in older adults with advanced cancer.
      ]. Only one study found no significant association between age and use of palliative care services [
      • Kumar P
      • Casarett D
      • Corcoran A
      • Desai K
      • Li Q
      • Chen J
      • et al.
      Utilization of supportive and palliative care services among oncology outpatients at one academic cancer center: determinants of use and barriers to access.
      ].

      3.4.1.2 Gender

      Nine studies examined the association between gender and palliative/hospice care utilization [
      • Burge FI
      • Lawson BJ
      • Johnston GM
      • Grunfeld E
      A population-based study of age inequalities in access to palliative care among cancer patients.
      ,
      • Lackan NA
      • Ostir GV
      • Freeman JL
      • Mahnken JD
      • Goodwin JS
      Decreasing variation in the use of hospice among older adults with breast, colorectal, lung, and prostate cancer.
      ,
      • Lackan NA
      • Ostir GV
      • Kuo YF
      • Freeman JL
      The association of marital status and hospice use in the USA.
      ,
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Phillips RS
      Barriers to hospice care among older patients dying with lung and colorectal cancer.
      ,
      • Miesfeldt S
      • Murray K
      • Lucas L
      • Chang CH
      • Goodman D
      • Morden NE
      Association of age, gender, and race with intensity of end-of-life care for medicare beneficiaries with cancer.
      ,
      • Nayar P
      • Qiu F
      • Watanabe-Galloway S
      • Boilesen E
      • Wang H
      • Lander L
      • et al.
      Disparities in end of life care for elderly lung cancer patients.
      ,
      • Tramontano AC
      • Nipp R
      • Kong CY
      • Yerramilli D
      • Gainor JF
      • Hur C
      Hospice use and end-of-life care among older patients with esophageal cancer.
      ,
      • Saito AM
      • Landrum MB
      • Neville BA
      • Ayanian JZ
      • Weeks JC
      • Earle CC
      Hospice care and survival among elderly patients with lung cancer.
      ,
      • Shugarman LR
      • Bird CE
      • Schuster CR
      • Lynn J
      Age and gender differences in medicare expenditures and service utilization at the end of life for lung cancer decedents.
      ]. There was a consistent finding that males were less likely to utilize hospice care services compared to their female counterparts.

      3.4.1.3 Race

      Thirteen studies examined the association between race/ethnicity and palliative/hospice care utilization [
      • Burge FI
      • Lawson BJ
      • Johnston GM
      • Grunfeld E
      A population-based study of age inequalities in access to palliative care among cancer patients.
      ,
      • Moher D
      • Liberati A
      • Tetzlaff J
      • Altman DG
      • Prisma Group
      Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.
      ,
      • Kumar P
      • Casarett D
      • Corcoran A
      • Desai K
      • Li Q
      • Chen J
      • et al.
      Utilization of supportive and palliative care services among oncology outpatients at one academic cancer center: determinants of use and barriers to access.
      ,
      • Hardy D
      • Chan W
      • Liu CC
      • Cormier JN
      • Xia R
      • Bruera E
      • et al.
      Racial disparities in the use of hospice services according to geographic residence and socioeconomic status in an elderly cohort with nonsmall cell lung cancer.
      ,
      • Lackan NA
      • Freeman JL
      • Goodwin JS
      Hospice use by older women dying with breast cancer between 1991 and 1996.
      ,
      • Ngo-Metzger Q
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Li FP
      • Phillips RS
      Older Asian Americans and Pacific Islanders dying of cancer use hospice less frequently than older white patients.
      ,
      • Lackan NA
      • Ostir GV
      • Freeman JL
      • Mahnken JD
      • Goodwin JS
      Decreasing variation in the use of hospice among older adults with breast, colorectal, lung, and prostate cancer.
      ,
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Phillips RS
      Barriers to hospice care among older patients dying with lung and colorectal cancer.
      ,
      • Nayar P
      • Qiu F
      • Watanabe-Galloway S
      • Boilesen E
      • Wang H
      • Lander L
      • et al.
      Disparities in end of life care for elderly lung cancer patients.
      ,
      • Smith AK
      • Earle CC
      • McCarthy EP
      Racial and ethnic differences in end-of-life care in fee-for-service medicare beneficiaries with advanced cancer.
      ,
      • Tramontano AC
      • Nipp R
      • Kong CY
      • Yerramilli D
      • Gainor JF
      • Hur C
      Hospice use and end-of-life care among older patients with esophageal cancer.
      ,
      • Gani F
      • Enumah ZO
      • Conca-Cheng AM
      • Canner JK
      • Johnston FM
      Palliative care utilization among patients admitted for gastrointestinal and thoracic cancers.
      ,
      • Saito AM
      • Landrum MB
      • Neville BA
      • Ayanian JZ
      • Weeks JC
      • Earle CC
      Hospice care and survival among elderly patients with lung cancer.
      ]. Most studies consistently found that racial minority (i.e. Black, Asian, and Pacific Islanders) were less likely to use hospice care services compared to White [
      • Burge FI
      • Lawson BJ
      • Johnston GM
      • Grunfeld E
      A population-based study of age inequalities in access to palliative care among cancer patients.
      ,
      • Moher D
      • Liberati A
      • Tetzlaff J
      • Altman DG
      • Prisma Group
      Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.
      ,
      • Hardy D
      • Chan W
      • Liu CC
      • Cormier JN
      • Xia R
      • Bruera E
      • et al.
      Racial disparities in the use of hospice services according to geographic residence and socioeconomic status in an elderly cohort with nonsmall cell lung cancer.
      ,
      • Ngo-Metzger Q
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Li FP
      • Phillips RS
      Older Asian Americans and Pacific Islanders dying of cancer use hospice less frequently than older white patients.
      ,
      • Lackan NA
      • Ostir GV
      • Freeman JL
      • Mahnken JD
      • Goodwin JS
      Decreasing variation in the use of hospice among older adults with breast, colorectal, lung, and prostate cancer.
      ,
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Phillips RS
      Barriers to hospice care among older patients dying with lung and colorectal cancer.
      ,
      • Nayar P
      • Qiu F
      • Watanabe-Galloway S
      • Boilesen E
      • Wang H
      • Lander L
      • et al.
      Disparities in end of life care for elderly lung cancer patients.
      ,
      • Smith AK
      • Earle CC
      • McCarthy EP
      Racial and ethnic differences in end-of-life care in fee-for-service medicare beneficiaries with advanced cancer.
      ,
      • Tramontano AC
      • Nipp R
      • Kong CY
      • Yerramilli D
      • Gainor JF
      • Hur C
      Hospice use and end-of-life care among older patients with esophageal cancer.
      ,
      • Saito AM
      • Landrum MB
      • Neville BA
      • Ayanian JZ
      • Weeks JC
      • Earle CC
      Hospice care and survival among elderly patients with lung cancer.
      ]. However, one study reported that being racial minority was associated with greater odds of receiving palliative care [
      • Gani F
      • Enumah ZO
      • Conca-Cheng AM
      • Canner JK
      • Johnston FM
      Palliative care utilization among patients admitted for gastrointestinal and thoracic cancers.
      ] and two studies reported that there was no significant association between race/ethnicity and palliative/hospice care utilization [
      • Kumar P
      • Casarett D
      • Corcoran A
      • Desai K
      • Li Q
      • Chen J
      • et al.
      Utilization of supportive and palliative care services among oncology outpatients at one academic cancer center: determinants of use and barriers to access.
      ,
      • Lackan NA
      • Freeman JL
      • Goodwin JS
      Hospice use by older women dying with breast cancer between 1991 and 1996.
      ].

      3.4.1.4 Marital status

      Six studies examined the association between marital status and palliative/hospice care utilization [
      • Kumar P
      • Casarett D
      • Corcoran A
      • Desai K
      • Li Q
      • Chen J
      • et al.
      Utilization of supportive and palliative care services among oncology outpatients at one academic cancer center: determinants of use and barriers to access.
      ,
      • Lackan NA
      • Freeman JL
      • Goodwin JS
      Hospice use by older women dying with breast cancer between 1991 and 1996.
      ,
      • Lackan NA
      • Ostir GV
      • Freeman JL
      • Mahnken JD
      • Goodwin JS
      Decreasing variation in the use of hospice among older adults with breast, colorectal, lung, and prostate cancer.
      ,
      • Lackan NA
      • Ostir GV
      • Kuo YF
      • Freeman JL
      The association of marital status and hospice use in the USA.
      ,
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Phillips RS
      Barriers to hospice care among older patients dying with lung and colorectal cancer.
      ,
      • Sharma N
      • Sharma AM
      • Wojtowycz MA
      • Wang D
      • Gajra A
      Utilization of palliative care and acute care services in older adults with advanced cancer.
      ] and consistently found that unmarried individuals were less likely to use palliative/hospice care services compared to their married counterparts with the exception of two studies [
      • Kumar P
      • Casarett D
      • Corcoran A
      • Desai K
      • Li Q
      • Chen J
      • et al.
      Utilization of supportive and palliative care services among oncology outpatients at one academic cancer center: determinants of use and barriers to access.
      ,
      • Sharma N
      • Sharma AM
      • Wojtowycz MA
      • Wang D
      • Gajra A
      Utilization of palliative care and acute care services in older adults with advanced cancer.
      ] that did not find any significant association between marital status and utilization of palliative/hospice care services.

      3.4.1.5 Socio-economic status (SES)

      Ten studies examined the association between SES and palliative/hospice care utilization [
      • Burge FI
      • Lawson BJ
      • Johnston GM
      • Grunfeld E
      A population-based study of age inequalities in access to palliative care among cancer patients.
      ,
      • Kumar P
      • Casarett D
      • Corcoran A
      • Desai K
      • Li Q
      • Chen J
      • et al.
      Utilization of supportive and palliative care services among oncology outpatients at one academic cancer center: determinants of use and barriers to access.
      ,
      • Hardy D
      • Chan W
      • Liu CC
      • Cormier JN
      • Xia R
      • Bruera E
      • et al.
      Racial disparities in the use of hospice services according to geographic residence and socioeconomic status in an elderly cohort with nonsmall cell lung cancer.
      ,
      • Ngo-Metzger Q
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Li FP
      • Phillips RS
      Older Asian Americans and Pacific Islanders dying of cancer use hospice less frequently than older white patients.
      ,
      • Lackan NA
      • Ostir GV
      • Freeman JL
      • Mahnken JD
      • Goodwin JS
      Decreasing variation in the use of hospice among older adults with breast, colorectal, lung, and prostate cancer.
      ,
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Phillips RS
      Barriers to hospice care among older patients dying with lung and colorectal cancer.
      ,
      • Nayar P
      • Qiu F
      • Watanabe-Galloway S
      • Boilesen E
      • Wang H
      • Lander L
      • et al.
      Disparities in end of life care for elderly lung cancer patients.
      ,
      • Tramontano AC
      • Nipp R
      • Kong CY
      • Yerramilli D
      • Gainor JF
      • Hur C
      Hospice use and end-of-life care among older patients with esophageal cancer.
      ,
      • Watanabe-Galloway S
      • Zhang W
      • Watkins K
      • Islam KM
      • Nayar P
      • Boilesen E
      • et al.
      Quality of end-of-life care among rural medicare beneficiaries with colorectal cancer.
      ,
      • Saito AM
      • Landrum MB
      • Neville BA
      • Ayanian JZ
      • Weeks JC
      • Earle CC
      Hospice care and survival among elderly patients with lung cancer.
      ]. There was a consistent finding that patients with low SES were less likely to use hospice care compared to patients with high SES. McCarthy et al. [
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Phillips RS
      Barriers to hospice care among older patients dying with lung and colorectal cancer.
      ] found that patients with higher median household income were more likely to use hospice care services compared to those with low household income. Burge et al. [
      • Burge FI
      • Lawson BJ
      • Johnston GM
      • Grunfeld E
      A population-based study of age inequalities in access to palliative care among cancer patients.
      ] examined the impact of educational status on palliative/hospice care utilization and found that less educated individuals were less likely to use palliative/hospice care services. Lackan et al. [
      • Lackan NA
      • Ostir GV
      • Freeman JL
      • Mahnken JD
      • Goodwin JS
      Decreasing variation in the use of hospice among older adults with breast, colorectal, lung, and prostate cancer.
      ] found that individuals residing in areas with low income and with lower educational levels were less likely to utilize hospice care services. Similarly, Lackan et al. [
      • Lackan NA
      • Freeman JL
      • Goodwin JS
      Hospice use by older women dying with breast cancer between 1991 and 1996.
      ] also found that women who lived in areas with low income and had lower education were less likely to be enrolled in hospice care services. Kumar et al. [
      • Kumar P
      • Casarett D
      • Corcoran A
      • Desai K
      • Li Q
      • Chen J
      • et al.
      Utilization of supportive and palliative care services among oncology outpatients at one academic cancer center: determinants of use and barriers to access.
      ] also examined the association of education and use of palliative and supportive care services and found that individuals with lower educational level (college graduates) had lower use of palliative and supportive care services. Hardy et al. [
      • Hardy D
      • Chan W
      • Liu CC
      • Cormier JN
      • Xia R
      • Bruera E
      • et al.
      Racial disparities in the use of hospice services according to geographic residence and socioeconomic status in an elderly cohort with nonsmall cell lung cancer.
      ] found that patients in poorest SES quartiles were less likely to receive hospice care services.

      3.4.1.6 Geographical residence

      Nine studies examined the relationship between geographical residence (rural versus urban) and palliative/hospice care utilization [
      • Burge FI
      • Lawson BJ
      • Johnston GM
      • Grunfeld E
      A population-based study of age inequalities in access to palliative care among cancer patients.
      ,
      • Lackan NA
      • Freeman JL
      • Goodwin JS
      Hospice use by older women dying with breast cancer between 1991 and 1996.
      ,
      • Ngo-Metzger Q
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Li FP
      • Phillips RS
      Older Asian Americans and Pacific Islanders dying of cancer use hospice less frequently than older white patients.
      ,
      • Lackan NA
      • Ostir GV
      • Freeman JL
      • Mahnken JD
      • Goodwin JS
      Decreasing variation in the use of hospice among older adults with breast, colorectal, lung, and prostate cancer.
      ,
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Phillips RS
      Barriers to hospice care among older patients dying with lung and colorectal cancer.
      ,
      • Nayar P
      • Qiu F
      • Watanabe-Galloway S
      • Boilesen E
      • Wang H
      • Lander L
      • et al.
      Disparities in end of life care for elderly lung cancer patients.
      ,
      • Tramontano AC
      • Nipp R
      • Kong CY
      • Yerramilli D
      • Gainor JF
      • Hur C
      Hospice use and end-of-life care among older patients with esophageal cancer.
      ,
      • Watanabe-Galloway S
      • Zhang W
      • Watkins K
      • Islam KM
      • Nayar P
      • Boilesen E
      • et al.
      Quality of end-of-life care among rural medicare beneficiaries with colorectal cancer.
      ,
      • Saito AM
      • Landrum MB
      • Neville BA
      • Ayanian JZ
      • Weeks JC
      • Earle CC
      Hospice care and survival among elderly patients with lung cancer.
      ]. The researchers consistently reported that individuals residing in rural areas were less likely to use palliative/hospice care services compared to individuals who resided in urban/metro areas. The reason for rural patients being less likely to use services was mostly distance to the facilities and access to those services.

      3.4.2 Provider-related barriers

      One study reported common barriers that older adults with cancer experienced in their oncological encounters and their need for supportive care interventions. In this mixed method study, semi-structured interviews yielded an in-depth understanding of barriers in cancer/EoL care. After interviewing 14 patients and reaching a thematic saturation, authors found that not feeling connected to their providers hindered patient involvement or participation in decision making processes, and ultimately influenced the results of communication [
      • Noordman J
      • Driesenaar JA
      • Henselmans I
      • Verboom J
      • Heijmans M
      • van Dulmen S
      Patient participation during oncological encounters: barriers and need for supportive interventions experienced by elderly cancer patients.
      ]. Additionally, other patients perceived a barrier to decision making or care decision was the feeling of not being taken seriously by their providers, or feeling they were not informed enough about available care choices (e.g., hospice transfer) or treatment options (e.g., palliative focused treatments) for their condition.

      3.4.3 Health insurance-related barriers

      This category includes studies examining health insurance and other policy and reimbursement issues. Four studies compared palliative/hospice care utilization based on type of health insurance [
      • Lackan NA
      • Ostir GV
      • Freeman JL
      • Mahnken JD
      • Goodwin JS
      Decreasing variation in the use of hospice among older adults with breast, colorectal, lung, and prostate cancer.
      ,
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Phillips RS
      Barriers to hospice care among older patients dying with lung and colorectal cancer.
      ,
      • Gani F
      • Enumah ZO
      • Conca-Cheng AM
      • Canner JK
      • Johnston FM
      Palliative care utilization among patients admitted for gastrointestinal and thoracic cancers.
      ,
      • Gidwani R
      • Joyce N
      • Kinosian B
      • Faricy-Anderson K
      • Levy C
      • Miller SC
      • et al.
      Gap between recommendations and practice of palliative care and hospice in cancer patients.
      ]. Two studies [
      • Lackan NA
      • Ostir GV
      • Freeman JL
      • Mahnken JD
      • Goodwin JS
      Decreasing variation in the use of hospice among older adults with breast, colorectal, lung, and prostate cancer.
      ,
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Phillips RS
      Barriers to hospice care among older patients dying with lung and colorectal cancer.
      ] compared the proportion of hospice care utilization in older adults with cancer between managed care enrollees and fee-for-service (FFS) enrollees. Lackan and colleagues examined a total of 170,136 older adults with cancer and found that 51,345 (30.2%) patients utilized hospice care prior to their deaths, across two groups. The proportion of hospice care recipients were lower among FFS insurance (28.3%) compared to those who were enrolled in managed care (42.2%), and the difference was statistically significant (p < 0.0001) [
      • Lackan NA
      • Ostir GV
      • Freeman JL
      • Mahnken JD
      • Goodwin JS
      Decreasing variation in the use of hospice among older adults with breast, colorectal, lung, and prostate cancer.
      ]. Similar findings were also reported in another study. McCarthy and colleagues examined 28,082 adults with cancer primarily patients with either lung cancer or colorectal cancer for whom hospice services were utilized [
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Phillips RS
      Barriers to hospice care among older patients dying with lung and colorectal cancer.
      ]. The study found only 25% (n = 41,888) from FFS group received hospice care in the lung cancer group while 40% (n = 6700) of managed care insurance enrollees received hospice care. In colorectal cancer group, only 19% (n = 2153) from FFS group received hospice care while 30% (n = 3400) of managed-care enrollees did [
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Phillips RS
      Barriers to hospice care among older patients dying with lung and colorectal cancer.
      ]. Gani et al. [
      • Gani F
      • Enumah ZO
      • Conca-Cheng AM
      • Canner JK
      • Johnston FM
      Palliative care utilization among patients admitted for gastrointestinal and thoracic cancers.
      ] examined palliative care utilization in patients admitted for gastrointestinal and thoracic cancer and found that patients enrolled in other type of health insurance (Medicaid, private insurance) were less likely to receive palliative care compared to patients with Medicare (53.8%, p < 0.001). Similarly, Gidwani et al. (2018) examined palliative and hospice care utilization in veterans who died of cancer in 2012 and found that patients with VA hospice care were significantly less likely to receive hospice care for at least three days compared to those who received VA-Purchased or Medicare hospice care [
      • Gidwani R
      • Joyce N
      • Kinosian B
      • Faricy-Anderson K
      • Levy C
      • Miller SC
      • et al.
      Gap between recommendations and practice of palliative care and hospice in cancer patients.
      ].

      4. Discussion

      Palliative and hospice care services play a major role in the management of patients with cancer. Evidence suggests these services are mostly underutilized among older adults with cancer. Therefore, a systematic review of existing literature to identify the barriers to palliative or hospice care utilization among older patients with cancer was critical. To our knowledge, this is the first study to synthesize barriers to palliative/hospice care utilization in this patient population.
      Among the 19 studies identified in this review, 17 studies were quantitative retrospective studies, one study was a cross-sectional study and one was mixed methods study, which are level 4 evidence. Longitudinal, prospective research on this topic is necessary to provide a higher level of evidence and evaluate the longitudinal impact of these factors. In terms of the type of services examined, four studies examined palliative care [
      • Burge FI
      • Lawson BJ
      • Johnston GM
      • Grunfeld E
      A population-based study of age inequalities in access to palliative care among cancer patients.
      ,
      • Kumar P
      • Casarett D
      • Corcoran A
      • Desai K
      • Li Q
      • Chen J
      • et al.
      Utilization of supportive and palliative care services among oncology outpatients at one academic cancer center: determinants of use and barriers to access.
      ,
      • Noordman J
      • Driesenaar JA
      • Henselmans I
      • Verboom J
      • Heijmans M
      • van Dulmen S
      Patient participation during oncological encounters: barriers and need for supportive interventions experienced by elderly cancer patients.
      ,
      • Gani F
      • Enumah ZO
      • Conca-Cheng AM
      • Canner JK
      • Johnston FM
      Palliative care utilization among patients admitted for gastrointestinal and thoracic cancers.
      ], one study examined both [
      • Gidwani R
      • Joyce N
      • Kinosian B
      • Faricy-Anderson K
      • Levy C
      • Miller SC
      • et al.
      Gap between recommendations and practice of palliative care and hospice in cancer patients.
      ] and the rest of the studies examined hospice care. Even though the importance and recommendations for palliative care has gained momentum in the past few years, the evidence on palliative care utilization in older adults with cancer still seems to be lacking.
      In addition, the sample s largely homogeneous with 10 out of the 18 studies analyzing data from the SEER-Medicare database. While the dataset contained large sample size, the participants were from the same sample pool in the US. More studies need to be conducted from diverse population to improve the generalizability of these findings.
      The socio-demographic variables examined by the studies included in this review included age, race, gender, marital status, socio-economic status, and geographical residence. Age and race were the most examined socio-demographic variables in these studies. Majority of the studies found that, racial minority (Black, Asian, Hispanics), male gender, being unmarried, low socio-economic condition, and rural residence served as barriers to palliative/hospice care utilization. Age showed mixed results in use of palliative or hospice care. These factors help identify high-risk population to promote the use of palliative/hospice care. Notably, the findings were all from quantitative results. Future research may further examine these demographic factors in qualitative research to further examine how these factors influence the use of palliative/hospice care and identify the facilitators and barriers to the care.
      Only one study examined patients' perception of provider-related barriers and identified the communication challenges that older patients with cancer experience as a barrier when interacting with their providers [
      • Noordman J
      • Driesenaar JA
      • Henselmans I
      • Verboom J
      • Heijmans M
      • van Dulmen S
      Patient participation during oncological encounters: barriers and need for supportive interventions experienced by elderly cancer patients.
      ]. The study found that patients did not feel connected to their providers and as a result had difficulties in communicating with their health care providers and participate in decision-making. Patients reported feeling not taken seriously by the providers and not informed about available care choices (i.e., palliative or hospice care) [
      • Noordman J
      • Driesenaar JA
      • Henselmans I
      • Verboom J
      • Heijmans M
      • van Dulmen S
      Patient participation during oncological encounters: barriers and need for supportive interventions experienced by elderly cancer patients.
      ]. This may contribute to lack of understanding of use of palliative or hospice care and the process to access the care. This points out the need for training for healthcare professional in communicating with family and patients with cancer. In addition, the discussion of care choice needs to be incorporated in the care process. However, data related to these provider-related barriers were obtained from qualitative interviews conducted with small sample size and only from the patient perspective. Other provider factors need to be explored by quantitative and qualitative approaches, such as provider's perception and training in palliative or hospice care, provider discipline, type of care settings, and the process of care for people with cancer. Also, to better understand the issue, provider and patient perspectives both need to be included.
      Only four studies examined the influence of health insurance in palliative/hospice care utilization [
      • Lackan NA
      • Ostir GV
      • Freeman JL
      • Mahnken JD
      • Goodwin JS
      Decreasing variation in the use of hospice among older adults with breast, colorectal, lung, and prostate cancer.
      ,
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Phillips RS
      Barriers to hospice care among older patients dying with lung and colorectal cancer.
      ,
      • Gani F
      • Enumah ZO
      • Conca-Cheng AM
      • Canner JK
      • Johnston FM
      Palliative care utilization among patients admitted for gastrointestinal and thoracic cancers.
      ,
      • Gidwani R
      • Joyce N
      • Kinosian B
      • Faricy-Anderson K
      • Levy C
      • Miller SC
      • et al.
      Gap between recommendations and practice of palliative care and hospice in cancer patients.
      ]. Two studies [
      • Lackan NA
      • Ostir GV
      • Freeman JL
      • Mahnken JD
      • Goodwin JS
      Decreasing variation in the use of hospice among older adults with breast, colorectal, lung, and prostate cancer.
      ,
      • McCarthy EP
      • Burns RB
      • Davis RB
      • Phillips RS
      Barriers to hospice care among older patients dying with lung and colorectal cancer.
      ] found that the proportion of hospice care recipients were higher among those who were enrolled in managed care compared to enrollees in FFS insurance. The results may be explained by two reasons. First, the patients enrolled in managed care often tend to be younger and accepting of new technologies much earlier compared to the older counterparts. Second, because of capitated reimbursement in managed care, providers may offer hospice care more often than their FSS counterparts [
      • Lackan NA
      • Ostir GV
      • Freeman JL
      • Mahnken JD
      • Goodwin JS
      Decreasing variation in the use of hospice among older adults with breast, colorectal, lung, and prostate cancer.
      ]. Two other studies [
      • Gani F
      • Enumah ZO
      • Conca-Cheng AM
      • Canner JK
      • Johnston FM
      Palliative care utilization among patients admitted for gastrointestinal and thoracic cancers.
      ,
      • Gidwani R
      • Joyce N
      • Kinosian B
      • Faricy-Anderson K
      • Levy C
      • Miller SC
      • et al.
      Gap between recommendations and practice of palliative care and hospice in cancer patients.
      ] found that patients with Medicare were more likely to receive palliative care/hospice care compared to those with other insurance (Medicaid, private insurance). These findings point out the important role insurance plays in utilization of palliative/hospice care. This needs to be further examined to identify the facilitators and barriers of the care.
      With the transformation of the health system, palliative/hospice care is being increasingly recognized as critical component of cancer care. This study demonstrates that there are certain factors that act as a barrier to timely and optimal utilization of palliative and hospice care. The factors associated with palliative or hospice care utilization in this review were mostly socio-demographic factors such as race, gender, marital status, socio-economic status, geographic residence and health insurance factors. Apart from these socio-demographic factors, evidence suggests several other barriers exist to integration of palliative care early in the disease trajectory such as negative stereotypes from patient and families [
      • Zimmermann C
      • Swami N
      • Krzyzanowska M
      • Leighl N
      • Rydall A
      • Rodin G
      • et al.
      Perceptions of palliative care among patients with advanced cancer and their caregivers.
      ], lack of knowledge on the difference between palliative and hospice care services, misconception that discussion about hospice care would take away hopes, and lack of knowledge on prognostication and timing of palliative care [
      • Dalgaard KM
      • Bergenholtz H
      • Nielsen ME
      • Timm H
      Early integration of palliative care in hospitals: a systematic review on methods, barriers, and outcome.
      ,
      • Hui D
      • Kim YJ
      • Park JC
      • Zhang Y
      • Strasser F
      • Cherny N
      • et al.
      Integration of oncology and palliative care: a systematic review.
      ]. As a result, providers often refer patients to palliative care services late in the disease trajectory when the patients experience uncontrollable symptoms and approach the end of life [
      • Charalambous H
      • Pallis A
      • Hasan B
      • O’Brien M
      Attitudes and referral patterns of lung cancer specialists in Europe to Specialized Palliative Care (SPC) and the practice of Early Palliative Care (EPC).
      ,
      • Wentlandt K
      • Krzyzanowska MK
      • Swami N
      • Rodin GM
      • Le LW
      • Zimmermann C
      Referral practices of oncologists to specialized palliative care.
      ]. However, these studies are not conducted specifically in an older population. Future studies should be conducted to understand older adults with cancer and their family's perspectives on the barriers to palliative and hospice care utilization.

      4.1 Study implications

      The findings of this review have some implications in policy and practice. Older adults with cancer are at risk for underutilization of palliative and hospice care services. Older adults who are single, ethnic minority, lower income, less educated, and live in rural areas are even at higher risk to underutilize palliative or hospice care. Therefore, older adults with cancer who may benefit from palliative care services should be identified and referred early in the disease trajectory. Providers and patients have communication challenges regarding open discussion about palliative care services, which leads to late referral and underutilization of these services. Therefore, interventions are needed to address provider-related barriers and communication challenges between the two parties and improve the utilization of palliative and hospice care services. Providing education to providers and patient population is important to improve awareness and increased utilization of palliative and hospice care services. FFS enrollees tend to be less likely to use palliative or hospice care. The reimbursement of FFS on use of palliative or hospice care needs to be further examined and payment gaps need to be identified. Better reimbursement policies need to be formulated in order to offer palliative and hospice care services in a lower cost to targeted older oncology patients.
      Findings from this systematic review can provide directions to future research. First, this review found that most studies on this topic are retrospective secondary analysis and most of them are from the same dataset. In addition, barriers from the perspectives of patients and providers are lacking. Evidence from prospective studies would provide stronger evidence. Therefore, future studies should be prospective and include qualitative studies to understand patients' perspectives on the barriers to palliative and hospice care utilization in this patient population. Qualitative studies from caregivers, family, and patients would provide greater insight and voices from all parties to better understand the barriers of care.
      Second, this systematic review points out the need to explore more correlates of palliative/hospice care use. Since palliative or hospice care utilization can be multi-faceted and complex, future research should examine additional variables that can affect the utilization of palliative or hospice care utilization. For patient characteristics, health literacy of the patient and their families, perceptions of palliative/hospice care and social support are potential correlates that are worth exploring. There are only a few studies examining provider-related or insurance-related factors. Future research may further explore care providers' perception and knowledge on palliative care as well as patients' access and financial barrier to the services.
      Third, many of the included studies were relatively outdated. With the changing healthcare system, advancement of palliative/hospice care services and changes in health-insurance related policies, the findings of many of these studies may not translate to the current situation. Therefore, future studies need to be focused on older adult populations to compare the findings.

      4.2 Strengths and limitations of the study

      One major strength of this review is that the search, extraction, and writing of the article followed the PRISMA guidelines. The thorough literature search and careful systematic extraction of data by independent reviewers ensured the inclusion of all relevant studies. Through categorizing study design, sample, and outcomes for palliative and hospice care utilization, this systematic review provides direction for future projects.
      While this review was conducted in a rigorous approach, it has some limitations. The majority of the included studies were retrospective secondary analysis and did not examine prospectively or qualitatively the patients' perspectives on barriers to palliative or hospice care utilization. In addition, except for two studies, almost all studies were from the US. The two studies from outside the US were from countries that have advanced health care systems and have palliative care services available, therefore limiting the generalizability of the findings worldwide especially in the developing countries where palliative care is still at its infancy. The location of research is important for this topic because the availability of palliative/hospice care services, cost, and public acceptance of palliative/hospice care may differ between countries and cultural contexts. Finally, case studies, review papers, editorials and commentaries were excluded in this systematic review leading to a small number of articles.
      To address these limitations, future research should examine the barriers to palliative/hospice care utilization care from patients and caregivers' perspectives prospectively in a larger scale together with other parameters and determinants of health including symptom burden, illness perception, access to palliative care services, caregivers support/social support, self-efficacy, satisfaction with care, and quality of services provided, as well as patients' perception on barriers to care outcomes when palliative care is applied to older adults with cancer. Finally, studies should also be conducted in less developed countries with less advanced health care systems.

      5. Conclusion

      With the aging of baby boomer generation, the number of older adults with cancer is increasing in the US and beyond posing new challenges to the healthcare system, cancer care, and the delivery of palliative and hospice care services. With the increasing number of older adults with cancer, the unmet needs of patients with cancer and families will be increasing, jeopardizing their quality of life. Therefore, more research is needed focusing on geriatric population who have unique care needs with the increase in number of chronic conditions topped with cancer.
      This systematic review identified various socio-demographic, provider-related, and health insurance related barriers to palliative and hospice care utilization among older adults with cancer. Patient-related barriers can guide the identification of at-risk population for underutilization of hospice and palliative care. Interventions are needed to address provider-related barriers such as communication challenges. Nevertheless, before findings can be generalized, future research may further examine this topic through prospective studies in a larger scale, with a sound theoretical framework.

      Disclosure statement

      The authors report no conflicts of interest.

      Funding

      The author(s) received no financial support for this research.

      Description of authors' roles

      Study concepts: J Parajuli, A Tark, Y-L Jao & J. Hupcey
      Study design: J Parajuli, A Tark, Y-L Jao & J. Hupcey
      Data acquisition: J Parajuli, & A Tark
      Quality control of data and algorithms: J Parajuli, & A Tark
      Data analysis and interpretation: J Parajuli, A Tark, Y-L Jao & J. Hupcey
      Statistical analysis: J Parajuli, A Tark, Y-L Jao & J. Hupcey
      Manuscript preparation: J Parajuli, A Tark, Y-L Jao & J. Hupcey
      Manuscript editing: J Parajuli, A Tark, Y-L Jao & J. Hupcey
      Manuscript review: J Parajuli, A Tark, Y-L Jao & J. Hupcey

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