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Differences in urban and suburban/rural settings regarding care provision and barriers of cancer care for older adults during COVID-19

Differences in urban and suburban/rural settings regarding care provision and barriers of cancer... Purpose Care for older adults with cancer became more challenging during the COVID-19 pandemic, particularly in urban hotspots. This study examined the potential differences in healthcare providers’ provision of as well as barriers to cancer care for older adults with cancer between urban and suburban/rural settings. Methods Members of the Advocacy Committee of the Cancer and Aging Research Group, with the Association of Commu- nity Cancer Centers, surveyed multidisciplinary healthcare providers responsible for the direct care of patients with cancer. Respondents were recruited through organizational listservs, email blasts, and social media messages. Descriptive statistics and chi-square tests were used. Results Complete data was available from 271 respondents (urban (n = 144), suburban/rural (n = 127)). Most respondents were social workers (42, 44%) or medical doctors/advanced practice providers (34, 13%) in urban and suburban/rural set- tings, respectively. Twenty-four percent and 32.4% of urban-based providers reported “strongly considering” treatment delays among adults aged 76–85 and > 85, respectively, compared to 13% and 15.4% of suburban/rural providers (Ps = 0.048, 0.013). More urban-based providers reported they were inclined to prioritize treatment for younger adults over older adults than suburban/rural providers (10.4% vs. 3.1%, p = 0.04) during the pandemic. The top concerns reported were similar between the groups and related to patient safety, treatment delays, personal safety, and healthcare provider mental health. Conclusion These findings demonstr ate location-based differences in providers’ attitudes regarding care provision for older adults with cancer during the COVID-19 pandemic. Keywords Older adults · Geriatric oncology · COVID-19 · Rural · Urban · Healthcare providers Abbreviations Introduction CDC Centers for Disease Control and Prevention NCI The National Cancer Institute The COVID-19 pandemic has had a significant impact on PPE Personal protective equipment cancer care since the emergence of the virus in late 2019 [1]. CARG Cancer and Aging Research Group To date, there have been more than 606 million confirmed ACCC Association of Community Cancer Centers COVID-19 cases and more than 6 million deaths globally RUCA Rural-urban commuting area [2]. Older adults (age ≥ 65 years) with cancer have been par- MDs Medical doctors ticularly impacted by the pandemic [3–14]. Older survivors APPs Advanced practice providers of cancer who contract COVID-19 are more likely to present with greater symptom severity and have higher mortality compared to younger cancer survivors [3–5]. Cancer care provision to older adults is further complicated by the fact that older cancer survivors are often underrepresented in research and thus lack tailored, evidence-based guidelines informed by the distinctive needs of this population [15–18]. Consideration of demographic location is needed, given * Jessica L. Krok-Schoen disparities between cancer treatment in urban and rural Jessica.krok@osumc.edu settings, which have been documented in the literature. Extended author information available on the last page of the article Vol.:(0123456789) 1 3 78 Page 2 of 9 Supportive Care in Cancer (2023) 31:78 Current literature indicates that rural-dwelling cancer sur- Materials and methods vivors are more likely to be older, to experience higher mortality, have more advanced disease progression on In Spring 2020, members of the Advocacy Committee of presentation, and difficulty accessing adequate cancer the Cancer and Aging Research Group (CARG) and the care than urban-residing patients [19]. Such disparities are Association of Community Cancer Centers (ACCC) devel- reflected in the prioritization that targets improved rural oped a Qualtrics questionnaire for providers of direct care cancer care by the American Society of Clinical Oncology for people with cancer. The online questionnaire included (ASCO), the Centers for Disease Control and Prevention 20 items, three of which were open-ended questions, (CDC), and the National Cancer Institute (NCI) [20–22]. focusing on the care of older adults with cancer during the The increased reliance on telemedicine that many health- COVID-19 pandemic in a variety of settings (see Appen- care systems have adopted as a result of the pandemic dix 1 for questionnaire). Previous efforts highlighting the may have furthered these documented disparities, as digi- quantitative and qualitative results have been reported tal broadband access is less feasible in more rural locations [33, 34]. This paper reports the comparative analysis of [23–28]. the quantitative data by participant-reported urban and Additionally, investigation by demographic location of suburban/rural settings. Those practicing in suburban and cancer care providers’ perspectives in light of COVID-19 rural settings were combined due to lower sample sizes is pertinent, considering the devastating effects of the pan- compared to the urban settings as well as previous litera- demic in urban hotspots [29]. The risk of spread of COVID ture [35–37]. Zip and census codes were not collected to in these more densely populated areas has had a significant convert to rural–urban commuting area (RUCA) codes due impact on older survivors of cancer, as older adults resid- to the survey’s international distribution [38]. ing in urban areas are more likely to report disruptions to Participants were asked about the prioritization daily life compared to rural-dwelling older adults [19]. of treatment for different age groups of patients with Despite being rich in healthcare infrastructure, barriers cancer, factors associated with the prioritization or to care unique to urban settings exist including language rescheduling of cancer treatments, receipt of guid- barriers and unwelcoming healthcare facilities [30]. Rural ance for decision-making, and the existence or lack of settings also have unique barriers to care including lim- written guidelines regarding the management of older ited access to quality healthcare, struggles with healthcare adults with cancer during the COVID-19 pandemic. workforce retention, and lower availability of COVID-19 Other questions explored the top five safety concerns vaccinations, which negatively impact cancer care pro- related to COVID-19, barriers associated with the use vided to older adults [30, 31]. For example, Saelee et al. of telemedicine, and increased barriers observed among found that COVID-19 vaccination coverage with the first older people with cancer. Information about providers’ dose of the primary vaccination series was lower in rural professional history (years in providing care to patients (58.5%) than in urban counties (75.4%); these disparities with cancer, percentage of older patients, medical pro- have increased more than twofold since April 2021 [32]. fession/specialty, cancer program classification and set- Thus, examining the location of healthcare providers is ting) was collected. essential to understand the potential differences in their Potential respondents were recruited by emails sent provision of and barriers to cancer care for older adults. through four professional organizations’ listservs and Some research has examined healthcare provider per- email blasts (CARG, ACCC, Association of Oncology spectives, highlighting the fear, uncertainty, and frustra- Social Work, and Social Work Hospice and Palliative tion over inconsistent guidelines and messaging in the Care Network) as well as social media messaging (e.g., early weeks and months of the pandemic, including fear Facebook, Twitter). Individuals were eligible to par- of adequate supply of personal protective equipment (PPE) ticipate if they (1) provided care for adults with can- [33, 34]. To our knowledge, there is currently no literature cer, (2) participated in the study voluntarily, and (3) examining geriatric oncology provider perspectives during understood that the results may be reported in multiple the pandemic by location. Clinician perspectives provide publications. insight into factors affecting treatment and survivorship The online questionnaire was available from April 8, care, decision-making, and priorities due to the COVID- 2020, to May 1, 2020. The study was determined exempt 19 pandemic. Therefore, the objective of this study was by the University of Cincinnati Institutional Review Board to examine if healthcare providers’ provision of as well as no identifying information was included in the collected as barriers to cancer care for older adults with cancer dif- data. The data were analyzed using descriptive statistics fers between urban and suburban/rural settings through an (frequencies, percentages), and chi-square tests of inde- online questionnaire. pendence with IBM SPSS Statistics version 27.0. 1 3 Supportive Care in Cancer (2023) 31:78 Page 3 of 9 78 Results Prioritization and postponement of treatment Demographic characteristics Significant differences were found between urban and suburban/rural providers regarding their considerations in Complete data were available from 271 respondents prioritizing treatment for different age groups of patients with cancer. Urban providers reported higher inclinations (urban (n = 144), suburban/r ur al (n = 127)). Mos t respondents were social workers (46.5% urban, 45.7% (10.4%) than suburban/rural providers (3.1%) to prioritize treatment for younger patients over older adults (X = 6.09, suburban/rural) or medical doctors/advanced practice providers (45.8%, 22.0%) in urban and suburban/rural p = 0.048). Furthermore, when asked about postponing/ rescheduling treatment due to COVID-related concerns, settings, respectively. Suburban/rural providers had sig- nificantly more years of professional experience than based on age group, urban providers reported significantly higher consideration of postponing/rescheduling treatment urban providers (p = 0.033). Suburban/r ur al providers saw a significantly higher percentage of older adults for adults aged 31–55, 66–75, 76–85, and > 85 than their suburban/rural counterparts (Fig. 1). Specifically, 24.5% and than urban providers (p = 0.016). Lastly, urban provid- ers worked primarily within academic medical centers 32.4% of urban-based providers reported “strongly consid- ering” treatment delays among adults aged 76–85 and > 85, or National Cancer Institute Comprehensive Cancer Centers while suburban/urban providers worked within respectively, compared to 13.0% and 15.4% of suburban/ 2 2 rural providers (X = 6.09, p = 0.048; X = 10.85, p = 0.013, community cancer programs (p < 0.001). (Table 1). Table 1 Demographic Urban Suburban/rural p-value information of survey (n = 144) (n = 127) respondents (n = 271) n (%) n (%) US-based 126 (87.5) 124 (97.6) 0.007 Profession Medical doctor and advanced practice providers 66 (45.8) 28 (22.0) < 0.001 Social worker 67 (46.5) 58 (45.7) Administration/program leader 4 (2.8) 16 (12.7) Nurse navigator/navigator 9 (6.3) 5 (4.0) Multiple 5 (3.5) 12 (9.5) Other 17 (11.8) 21 (16.5) Number of years providing care to patients with cancer 1–4 35 (24.3) 21 (16.5) 0.033 5–10 38 (26.4) 27 (21.3) 11–20 43 (29.9) 35 (27.6) 20 + 28 (19.4) 44 (34.6) % of patients are older adults (age ≥ 65 years) < 10% 2 (1.4) 0 (0) 0.016 11–25% 9 (6.3) 3 (2.4) 26–50% 43 (30.1) 27 (21.3) 51–75% 69 (48.3) 86 (67.7) > 75% 20 (14.0) 11 (8.7) Classification Academic/NCI comprehensive cancer center 81 (56.3) 18 (14.2) < 0.001 Hospital 21 (14.6) 25 (19.7) Community cancer program 18 (12.5) 60 (47.2) Integrated 10 (6.9) 9 (7.1) Physician-owned oncology practice 4 (2.8) 1 (0.8) Other 9 (6.3) 7 (5.5) Oncologists, geriatricians, or advanced practice providers. Oncologists included medical, surgical, radia- tion, gynecologic, and geriatric specialties Includes oncology nurses, dieticians, case managers, palliative care workers, and medical assistants 1 3 78 Page 4 of 9 Supportive Care in Cancer (2023) 31:78 Urban Suburban/Rural 80 80 70 70 60 60 50 50 * * * * 40 40 30 30 20 20 10 10 0 0 <30 31-55 56-65 66-75 76-85 >85 <3031-55 56-6566-75 76-85 >85 Not considering Somewhat considering Not considering Somewhat considering Considering Strongly considering Considering Strongly considering Fig. 1 Consideration of postponing or rescheduling cancer treatment by age group among urban and suburban/rural providers. Note: * = p < 0.05. Specific p-values = 0.048, 0.020, 0.048, and 0.013 for 31–55, 66–75, 76–85, and > 85 age groups between urban and suburban/rural providers respectively). There was no significant difference in postpon- member access (e.g., family member attendance in clinic ing/rescheduling treatment due to COVID-related concerns, visits, hospital stays) (39.6% vs. 22.8%, respectively, among patients aged 56–65 between urban and suburban/ X = 8.74 p = 0.003), and psychosocial status (e.g., emo- rural providers. tional and social functioning) (38.2% vs. 25.2%, respec- Both urban and suburban/rural providers considered tively, X = 5.23, p = 0.022) at significantl y higher rates comorbidities, cancer stage, frailty, performance status than suburban/rural providers. (e.g., patient’s ability to perform certain activities of There was no difference by provider location regard- daily living without help), and age as their top five fac- ing specific written guidelines regarding the management tors in deciding to postpone/reschedule cancer treatment of older adults with cancer during the COVID-19 crisis during the pandemic (Table 2). However, urban provid- (X = 2.10, p = 0.43). Specifically, 52.8% and 58.7% of ers reported considering comorbidities (77.1% vs. 66.1%, urban and suburban/rural providers, respectively, reported respectively, X = 4.00, p = 0.045), life expectancy (47.9% no written guidelines and an additional 29.2% and 29.1% vs. 31.5%, respectively, X = 7.57 p = 0.006), family of urban and suburban/rural providers reported uncertainty of any written guidelines. Table 2 Patient characteristics Urban Sub/rural Chi- taken into account when n (%) n (%) square considering to postpone/ p-value reschedule cancer treatment during the COVID-19 pandemic Comorbidities 111 (77.1) 84 (66.1) 0.045 Cancer stage 106 (73.6) 85 (66.9) 0.229 Frailty 102 (70.8) 86 (67.7) 0.579 Performance status (patient’s ability to perform certain 88 (61.1) 67 (52.8) 0.165 activities of daily living without help) Age 78 (54.2) 55 (43.3) 0.074 Life expectancy 69 (47.9) 40 (31.5) 0.006 Family member access (family member attendance in clinic 57 (39.6) 29 (22.8) 0.003 visits, hospital stays) Psychosocial status (emotional and social functioning) 55 (38.2) 32 (25.2) 0.022 Transportation 52 (36.1) 38 (29.9) 0.280 Insurance 10 (6.9) 4 (3.1) 0.159 Employment 5 (3.5) 2 (1.6) 0.326 Other 25 (17.4) 23 (18.1) 0.872 1 3 Supportive Care in Cancer (2023) 31:78 Page 5 of 9 78 Safety concerns related to COVID‑19 Barriers to resources and telemedicine Overall, the top concerns related to COVID-19 Urban-based providers reported significantly higher reported were similar between the urban- and subur- observed increase of barriers regarding access to prescrip- ban-/rural-based providers (Table  3). The most com- tions (29.9% vs. 16.5%, respectively, X = 6.64, p = 0.010). mon concern was patient safety (81.9%, 85.8%) fol- Additionally, urban providers reported higher observed lowed by treatment delays (62.5%, 66.9%), healthcare increase of transportation barriers (74.3%) compared to their provider mental health (55.6%, 58.3%), and personal suburban/rural counterparts (68.5%, p = 0.178). Suburban-/ family safety (51.4%, 55.9%) among urban and sub- rural-based providers reported higher observed increase of urban-/rural-based providers, respectively. Signifi - barriers among older adults accessing food (33.9%) and car- cant differences were observed by location for two egiver availability (66.1%) compared to their urban coun- 2 2 safety concerns: supply of PPE and patient mental terparts (31.3% and 62.5%, X = 2.09, p = 0.70; X = 0.39, health. Suburban-/r ural-based providers repor ted sig- p = 0.53, respectively). nificantly higher concerns about the supply of PPE There were no significant differences by provider loca- (62.2%) compared to urban-based providers (49.3%) tion in reported increase of perceived barriers to using (X = 4.54, p = 0.022). Lastly, urban-based providers telemedicine with older adults with cancer (Table 4). The reported significantly higher concerns about patient most reported perceived barriers were patient access (e.g., mental health (55.6%) than suburban-/rural-based pro- no smart phone, internet access) (91%, 92.1%), patient not viders (42.5%) (X = 4.59, p = 0.032). being tech savvy (89.6%, 92.1%), and patient perception Table 3 Top 5 concerns related Concerns Urban Suburban/rural Chi- to COVID-19 reported by n (%) n (%) square urban- and suburban-based p-value providers Patient safety 118 (81.9) 109 (85.8) 0.413 Treatment delay 90 (62.5) 85 (66.9) 0.447 Healthcare provider mental health 80 (55.6) 74 (58.3) 0.653 Patient mental health 80 (55.6) 54 (42.5) 0.032 My family safety 74 (51.4) 71 (55.9) 0.457 Personal safety 72 (50.0) 60 (52.8) 0.651 Supply of personal protective equipment 71 (49.3) 79 (62.2) 0.022 Patient mortality 67 (46.5) 47 (37.0) 0.113 Family of patient safety 24 (16.7) 23 (18.1) 0.754 Research delays 20 (13.9) 10 (7.9) 0.115 Clinical trial accrual 5 (3.5) 4 (3.1) 0.882 Table 4 Providers’ reported Variable Urban Suburban/rural Chi- barriers to using telehealth with n (%) n (%) square older adults with cancer p-value Patient access (e.g., no smart phone or internet 131 (91.0) 117 (92.1) 0.734 access) Patient not tech savvy 129 (89.6) 117 (92.1) 0.470 Patient perception issues 58 (40.3) 63 (49.6) 0.123 Program/institution infrastructure 43 (29.9) 37 (29.1) 0.896 Healthcare worker technology challenges 35 (24.3) 40 (31.5) 0.187 Healthcare worker home-work issues 23 (16.0) 23 (18.1) 0.640 Healthcare worker preference/policy 19 (13.2) 12 (9.4) 0.334 Uncertainty of reimbursement 17 (11.8) 16 (12.6) 0.842 Other barriers 9 (6.3) 9 (7.1) 0.811 No barriers 4 (2.8) 0 (0) 0.058 1 3 78 Page 6 of 9 Supportive Care in Cancer (2023) 31:78 issues of telemedicine (40.3%, 49.6%) among urban- and safety. Significant differences were observed regarding suburban-/rural-based providers, respectively. patient mental health (higher in urban-based providers) and supply of PPE (higher in suburban-/rural-based providers). These differences may be attributed to limited resources by Discussion location. COVID-19 surged in urban areas with limited men- tal healthcare support (both informal and formal) despite This study examined whether healthcare providers’ provi- increased demand during the data collection period. Tel- sion of as well as barriers to care for older adults with cancer emedicine challenges at that period may have also negatively differed between urban and suburban/rural settings. Signifi- impacted patient mental health [46–48]. At the same time, cant differences were found between urban and suburban/ the need for PPE was concentrated and subsequently pri- rural providers regarding their considerations for prioritizing oritized to those areas of surge, away from suburban/rural treatment for different age groups of patients with cancer; areas, leaving these providers with less PPE than the urban- urban-based providers were more likely to prioritize treat- based providers [49, 50]. ment for younger patients than older patients. This result is Barriers to using telemedicine were commonly experi- most likely due to the timing of the survey, April 2020, when enced by both urban and suburban/rural providers. This find - major urban centers such as New York City were experienc- ing was expected and understandable given the sudden pro- ing high numbers of COVID-19 cases. In later months, cases liferation of telemedicine among adults with cancer. The use surged in suburban and rural settings [39]. Contrary to the of telemedicine by some estimates grew 30-fold in the USA current study’s findings regarding treatment prioritization and almost 100-fold in the Medicare population in the sec- in urban settings, McGuire and colleagues argued that, in ond quarter of 2020 compared to before the pandemic [51, suburban/rural areas, patients may be more vulnerable to 52]. Before COVID-19, research found that older adults are the economic and health impacts of a pandemic [40]. They more receptive to technology use than was typically assumed posited that rural healthcare providers are not only fewer [53–55]. For example, over two-thirds of older adults use in number than their urban counterparts, but also work the internet daily and more than half have home broadband with fewer resources, less public transportation, and deliv- service [56]. However, as evidenced by this study and oth- ery options. Another potential reason for the difference in ers, older adults using technology may have barriers to tel- treatment prioritization by provider location may be related emedicine use, including internet and device access, design to the ageist approach that older adults with cancer should challenges, privacy and trust concerns, and cost [57–60]. For not receive equal treatment [15, 41, 42]. Previous studies example, Lam and colleagues found many older adults may have found that the COVID-19 pandemic has accentuated be unable to take part in health-related video visits because the exclusion and prejudice against older adults, warrant- of disabilities or inexperience with technology [60]. Again, ing immediate intervention and education [15, 41, 43, 44]. the timing of this survey may have influenced the reported This ageist perspective observed in the current study may barriers regarding telemedicine. In Spring 2020, the roll-out have emerged in part by the lack of written guidelines for of telemedicine was rapidly implemented to ensure adequate the management of older adults with cancer experienced by continuity of care while minimizing exposure to COVID- more than half of the rural- and suburban-based providers. 19. As telemedicine care becomes more widely used, it An additional possibility is the perception that older adults provides an important opportunity to expand telemedicine are more likely to have comorbidities or be frail and, hence, care to older, rural patients who live a greater distance from have increased risk for cancer treatment toxicity during tertiary medical centers, or to those older adults who may COVID-19 [45]. The current study’s findings support this have transportation or mobility limitations. Regardless of notion; urban respondents considered comorbidities and life location, modifications to telemedicine geriatric assessment expectancy (77%, 48%) at significantly higher prevalence as well as video visits [61] are important for promoting posi- than their suburban/rural counterparts (66%, 32%, respec- tive patient outcomes and patient-provider relationships, tively). Additional information about the provider’s patient facilitating clear communication, and observing non-verbal populations (e.g., median age, cancer stage) and their insti- communication [62–65]. tution’s response to COVID-19 (e.g., guidelines, hospital strain) as well as their experience (e.g., geriatric specializa- Limitations tions, trainings) would provide context for better understand- ing of the inclinations to prioritize treatment for different age The first limitation was that suburban and rural provider’s groups of patients with cancer. responses were combined to facilitate adequate sample Provider concerns regarding COVID-19 were similar size compared to the sample size of urban-based providers. regardless of provider location. The most reported concerns There could be differences between the two settings such were patient safety, treatment delays, and personal/family as resources and the impact of COVID-19 at the time of 1 3 Supportive Care in Cancer (2023) 31:78 Page 7 of 9 78 Data Availability Due to its proprietary nature, supporting data cannot the survey. In addition, there was an uneven distribution of be made openly available. healthcare providers (MDs and APPs versus social workers) based on location, which may skew the findings to a psy - Declarations chosocial lens rather than a treatment decision-making lens. Similarly, significantly more suburban/rural providers than Ethics approval The study was determined exempt by the University of Cincinnati Institutional Review Board as no identifying information urban providers were US-based, which can bias compari- was included in the collected data. sons between urban and suburban/rural provider responses. 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Hargittai E, Piper AM, Morris MR (2019) From internet access to among persons with and without a cancer history: Establishing internet skills: digital inequality among older adults. Univ Access reliability and agreement with in-person assessment. J Geriatr Inf Soc 18(4):881–890 Oncol 13(5):691–697 58. Kruse C, Fohn J, Wilson N, Patlan EN, Zipp S, Mileski M (2020) Utilization barriers and medical outcomes commensurate with the Publisher's note Springer Nature remains neutral with regard to use of telehealth among older adults: systematic review. J Med jurisdictional claims in published maps and institutional affiliations. Internet Res 8(8):e20359 59. Roberts ET, Mehrotra A (2020) Assessment of disparities in Springer Nature or its licensor (e.g. a society or other partner) holds digital access among Medicare beneficiaries and implications for exclusive rights to this article under a publishing agreement with the telemedicine. JAMA Intern Med 180(10):1386–1389 author(s) or other rightsholder(s); author self-archiving of the accepted 60. Lam K, Lu AD, Shi Y, Covinsky KE (2020) Assessing telemedi- manuscript version of this article is solely governed by the terms of cine unreadiness among older adults in the United States during such publishing agreement and applicable law. the COVID-19 pandemic. JAMA Intern Med 180(10):1389–1391 Authors and Affiliations 1 2 3 4 5 Janell L. Pisegna  · Karlynn BrintzenhofeSzoc  · Armin Shahrokni  · Beverly Canin  · Elana Plotkin  · 5 6 7 8 9 Leigh M. Boehmer  · Leana Chien  · Mariuxi Viteri Malone  · Amy R. MacKenzie  · Jessica L. Krok‑Schoen Janell L. Pisegna System, University of Colorado Anschutz Medical Campus, janell.pisegna@cuanschutz.edu Aurora, CO, USA Karlynn BrintzenhofeSzoc Kent School of Social Work, University of Louisville, karlynn.brintzenhofeszoc@louisville.edu Louisville, KY, USA Armin Shahrokni Department of Medicine, Gastrointestinal Oncology shahroka@mskcc.org and Geriatrics Services, Memorial Sloan Kettering Cancer Center, New York, NY, USA Beverly Canin caninbeverly@gmail.com Cancer and Aging Research Group, Duarte, CA, USA Elana Plotkin Provider Education Programs, Association of Community EPlotkin@accc-cancer.org Cancer Centers, Rockville, Maryland, USA Leigh M. Boehmer City of Hope Comprehensive Cancer Center, Duarte, CA, lboehmer@accc-cancer.org USA Leana Chien Division of Hematology, Florida Cancer Specialists lchien@coh.org and Research Institute, Venice, FL, USA Mariuxi Viteri Malone Division of Hematology, Thomas Jefferson University, mariux.viteri@gmail.com Philadelphia, PA, USA Amy R. MacKenzie School of Health and Rehabilitation Sciences, College Amy.Mackenzie@jefferson.edu of Medicine, The Ohio State University, 453 W. 10Th Ave., Columbus, OH 43210, USA Physical Therapy Program, Geriatric Research Education and Clinical Center VA Eastern Colorado Healthcare 1 3 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Supportive Care in Cancer Pubmed Central

Differences in urban and suburban/rural settings regarding care provision and barriers of cancer care for older adults during COVID-19

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© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2022, Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
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1433-7339
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10.1007/s00520-022-07544-y
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Abstract

Purpose Care for older adults with cancer became more challenging during the COVID-19 pandemic, particularly in urban hotspots. This study examined the potential differences in healthcare providers’ provision of as well as barriers to cancer care for older adults with cancer between urban and suburban/rural settings. Methods Members of the Advocacy Committee of the Cancer and Aging Research Group, with the Association of Commu- nity Cancer Centers, surveyed multidisciplinary healthcare providers responsible for the direct care of patients with cancer. Respondents were recruited through organizational listservs, email blasts, and social media messages. Descriptive statistics and chi-square tests were used. Results Complete data was available from 271 respondents (urban (n = 144), suburban/rural (n = 127)). Most respondents were social workers (42, 44%) or medical doctors/advanced practice providers (34, 13%) in urban and suburban/rural set- tings, respectively. Twenty-four percent and 32.4% of urban-based providers reported “strongly considering” treatment delays among adults aged 76–85 and > 85, respectively, compared to 13% and 15.4% of suburban/rural providers (Ps = 0.048, 0.013). More urban-based providers reported they were inclined to prioritize treatment for younger adults over older adults than suburban/rural providers (10.4% vs. 3.1%, p = 0.04) during the pandemic. The top concerns reported were similar between the groups and related to patient safety, treatment delays, personal safety, and healthcare provider mental health. Conclusion These findings demonstr ate location-based differences in providers’ attitudes regarding care provision for older adults with cancer during the COVID-19 pandemic. Keywords Older adults · Geriatric oncology · COVID-19 · Rural · Urban · Healthcare providers Abbreviations Introduction CDC Centers for Disease Control and Prevention NCI The National Cancer Institute The COVID-19 pandemic has had a significant impact on PPE Personal protective equipment cancer care since the emergence of the virus in late 2019 [1]. CARG Cancer and Aging Research Group To date, there have been more than 606 million confirmed ACCC Association of Community Cancer Centers COVID-19 cases and more than 6 million deaths globally RUCA Rural-urban commuting area [2]. Older adults (age ≥ 65 years) with cancer have been par- MDs Medical doctors ticularly impacted by the pandemic [3–14]. Older survivors APPs Advanced practice providers of cancer who contract COVID-19 are more likely to present with greater symptom severity and have higher mortality compared to younger cancer survivors [3–5]. Cancer care provision to older adults is further complicated by the fact that older cancer survivors are often underrepresented in research and thus lack tailored, evidence-based guidelines informed by the distinctive needs of this population [15–18]. Consideration of demographic location is needed, given * Jessica L. Krok-Schoen disparities between cancer treatment in urban and rural Jessica.krok@osumc.edu settings, which have been documented in the literature. Extended author information available on the last page of the article Vol.:(0123456789) 1 3 78 Page 2 of 9 Supportive Care in Cancer (2023) 31:78 Current literature indicates that rural-dwelling cancer sur- Materials and methods vivors are more likely to be older, to experience higher mortality, have more advanced disease progression on In Spring 2020, members of the Advocacy Committee of presentation, and difficulty accessing adequate cancer the Cancer and Aging Research Group (CARG) and the care than urban-residing patients [19]. Such disparities are Association of Community Cancer Centers (ACCC) devel- reflected in the prioritization that targets improved rural oped a Qualtrics questionnaire for providers of direct care cancer care by the American Society of Clinical Oncology for people with cancer. The online questionnaire included (ASCO), the Centers for Disease Control and Prevention 20 items, three of which were open-ended questions, (CDC), and the National Cancer Institute (NCI) [20–22]. focusing on the care of older adults with cancer during the The increased reliance on telemedicine that many health- COVID-19 pandemic in a variety of settings (see Appen- care systems have adopted as a result of the pandemic dix 1 for questionnaire). Previous efforts highlighting the may have furthered these documented disparities, as digi- quantitative and qualitative results have been reported tal broadband access is less feasible in more rural locations [33, 34]. This paper reports the comparative analysis of [23–28]. the quantitative data by participant-reported urban and Additionally, investigation by demographic location of suburban/rural settings. Those practicing in suburban and cancer care providers’ perspectives in light of COVID-19 rural settings were combined due to lower sample sizes is pertinent, considering the devastating effects of the pan- compared to the urban settings as well as previous litera- demic in urban hotspots [29]. The risk of spread of COVID ture [35–37]. Zip and census codes were not collected to in these more densely populated areas has had a significant convert to rural–urban commuting area (RUCA) codes due impact on older survivors of cancer, as older adults resid- to the survey’s international distribution [38]. ing in urban areas are more likely to report disruptions to Participants were asked about the prioritization daily life compared to rural-dwelling older adults [19]. of treatment for different age groups of patients with Despite being rich in healthcare infrastructure, barriers cancer, factors associated with the prioritization or to care unique to urban settings exist including language rescheduling of cancer treatments, receipt of guid- barriers and unwelcoming healthcare facilities [30]. Rural ance for decision-making, and the existence or lack of settings also have unique barriers to care including lim- written guidelines regarding the management of older ited access to quality healthcare, struggles with healthcare adults with cancer during the COVID-19 pandemic. workforce retention, and lower availability of COVID-19 Other questions explored the top five safety concerns vaccinations, which negatively impact cancer care pro- related to COVID-19, barriers associated with the use vided to older adults [30, 31]. For example, Saelee et al. of telemedicine, and increased barriers observed among found that COVID-19 vaccination coverage with the first older people with cancer. Information about providers’ dose of the primary vaccination series was lower in rural professional history (years in providing care to patients (58.5%) than in urban counties (75.4%); these disparities with cancer, percentage of older patients, medical pro- have increased more than twofold since April 2021 [32]. fession/specialty, cancer program classification and set- Thus, examining the location of healthcare providers is ting) was collected. essential to understand the potential differences in their Potential respondents were recruited by emails sent provision of and barriers to cancer care for older adults. through four professional organizations’ listservs and Some research has examined healthcare provider per- email blasts (CARG, ACCC, Association of Oncology spectives, highlighting the fear, uncertainty, and frustra- Social Work, and Social Work Hospice and Palliative tion over inconsistent guidelines and messaging in the Care Network) as well as social media messaging (e.g., early weeks and months of the pandemic, including fear Facebook, Twitter). Individuals were eligible to par- of adequate supply of personal protective equipment (PPE) ticipate if they (1) provided care for adults with can- [33, 34]. To our knowledge, there is currently no literature cer, (2) participated in the study voluntarily, and (3) examining geriatric oncology provider perspectives during understood that the results may be reported in multiple the pandemic by location. Clinician perspectives provide publications. insight into factors affecting treatment and survivorship The online questionnaire was available from April 8, care, decision-making, and priorities due to the COVID- 2020, to May 1, 2020. The study was determined exempt 19 pandemic. Therefore, the objective of this study was by the University of Cincinnati Institutional Review Board to examine if healthcare providers’ provision of as well as no identifying information was included in the collected as barriers to cancer care for older adults with cancer dif- data. The data were analyzed using descriptive statistics fers between urban and suburban/rural settings through an (frequencies, percentages), and chi-square tests of inde- online questionnaire. pendence with IBM SPSS Statistics version 27.0. 1 3 Supportive Care in Cancer (2023) 31:78 Page 3 of 9 78 Results Prioritization and postponement of treatment Demographic characteristics Significant differences were found between urban and suburban/rural providers regarding their considerations in Complete data were available from 271 respondents prioritizing treatment for different age groups of patients with cancer. Urban providers reported higher inclinations (urban (n = 144), suburban/r ur al (n = 127)). Mos t respondents were social workers (46.5% urban, 45.7% (10.4%) than suburban/rural providers (3.1%) to prioritize treatment for younger patients over older adults (X = 6.09, suburban/rural) or medical doctors/advanced practice providers (45.8%, 22.0%) in urban and suburban/rural p = 0.048). Furthermore, when asked about postponing/ rescheduling treatment due to COVID-related concerns, settings, respectively. Suburban/rural providers had sig- nificantly more years of professional experience than based on age group, urban providers reported significantly higher consideration of postponing/rescheduling treatment urban providers (p = 0.033). Suburban/r ur al providers saw a significantly higher percentage of older adults for adults aged 31–55, 66–75, 76–85, and > 85 than their suburban/rural counterparts (Fig. 1). Specifically, 24.5% and than urban providers (p = 0.016). Lastly, urban provid- ers worked primarily within academic medical centers 32.4% of urban-based providers reported “strongly consid- ering” treatment delays among adults aged 76–85 and > 85, or National Cancer Institute Comprehensive Cancer Centers while suburban/urban providers worked within respectively, compared to 13.0% and 15.4% of suburban/ 2 2 rural providers (X = 6.09, p = 0.048; X = 10.85, p = 0.013, community cancer programs (p < 0.001). (Table 1). Table 1 Demographic Urban Suburban/rural p-value information of survey (n = 144) (n = 127) respondents (n = 271) n (%) n (%) US-based 126 (87.5) 124 (97.6) 0.007 Profession Medical doctor and advanced practice providers 66 (45.8) 28 (22.0) < 0.001 Social worker 67 (46.5) 58 (45.7) Administration/program leader 4 (2.8) 16 (12.7) Nurse navigator/navigator 9 (6.3) 5 (4.0) Multiple 5 (3.5) 12 (9.5) Other 17 (11.8) 21 (16.5) Number of years providing care to patients with cancer 1–4 35 (24.3) 21 (16.5) 0.033 5–10 38 (26.4) 27 (21.3) 11–20 43 (29.9) 35 (27.6) 20 + 28 (19.4) 44 (34.6) % of patients are older adults (age ≥ 65 years) < 10% 2 (1.4) 0 (0) 0.016 11–25% 9 (6.3) 3 (2.4) 26–50% 43 (30.1) 27 (21.3) 51–75% 69 (48.3) 86 (67.7) > 75% 20 (14.0) 11 (8.7) Classification Academic/NCI comprehensive cancer center 81 (56.3) 18 (14.2) < 0.001 Hospital 21 (14.6) 25 (19.7) Community cancer program 18 (12.5) 60 (47.2) Integrated 10 (6.9) 9 (7.1) Physician-owned oncology practice 4 (2.8) 1 (0.8) Other 9 (6.3) 7 (5.5) Oncologists, geriatricians, or advanced practice providers. Oncologists included medical, surgical, radia- tion, gynecologic, and geriatric specialties Includes oncology nurses, dieticians, case managers, palliative care workers, and medical assistants 1 3 78 Page 4 of 9 Supportive Care in Cancer (2023) 31:78 Urban Suburban/Rural 80 80 70 70 60 60 50 50 * * * * 40 40 30 30 20 20 10 10 0 0 <30 31-55 56-65 66-75 76-85 >85 <3031-55 56-6566-75 76-85 >85 Not considering Somewhat considering Not considering Somewhat considering Considering Strongly considering Considering Strongly considering Fig. 1 Consideration of postponing or rescheduling cancer treatment by age group among urban and suburban/rural providers. Note: * = p < 0.05. Specific p-values = 0.048, 0.020, 0.048, and 0.013 for 31–55, 66–75, 76–85, and > 85 age groups between urban and suburban/rural providers respectively). There was no significant difference in postpon- member access (e.g., family member attendance in clinic ing/rescheduling treatment due to COVID-related concerns, visits, hospital stays) (39.6% vs. 22.8%, respectively, among patients aged 56–65 between urban and suburban/ X = 8.74 p = 0.003), and psychosocial status (e.g., emo- rural providers. tional and social functioning) (38.2% vs. 25.2%, respec- Both urban and suburban/rural providers considered tively, X = 5.23, p = 0.022) at significantl y higher rates comorbidities, cancer stage, frailty, performance status than suburban/rural providers. (e.g., patient’s ability to perform certain activities of There was no difference by provider location regard- daily living without help), and age as their top five fac- ing specific written guidelines regarding the management tors in deciding to postpone/reschedule cancer treatment of older adults with cancer during the COVID-19 crisis during the pandemic (Table 2). However, urban provid- (X = 2.10, p = 0.43). Specifically, 52.8% and 58.7% of ers reported considering comorbidities (77.1% vs. 66.1%, urban and suburban/rural providers, respectively, reported respectively, X = 4.00, p = 0.045), life expectancy (47.9% no written guidelines and an additional 29.2% and 29.1% vs. 31.5%, respectively, X = 7.57 p = 0.006), family of urban and suburban/rural providers reported uncertainty of any written guidelines. Table 2 Patient characteristics Urban Sub/rural Chi- taken into account when n (%) n (%) square considering to postpone/ p-value reschedule cancer treatment during the COVID-19 pandemic Comorbidities 111 (77.1) 84 (66.1) 0.045 Cancer stage 106 (73.6) 85 (66.9) 0.229 Frailty 102 (70.8) 86 (67.7) 0.579 Performance status (patient’s ability to perform certain 88 (61.1) 67 (52.8) 0.165 activities of daily living without help) Age 78 (54.2) 55 (43.3) 0.074 Life expectancy 69 (47.9) 40 (31.5) 0.006 Family member access (family member attendance in clinic 57 (39.6) 29 (22.8) 0.003 visits, hospital stays) Psychosocial status (emotional and social functioning) 55 (38.2) 32 (25.2) 0.022 Transportation 52 (36.1) 38 (29.9) 0.280 Insurance 10 (6.9) 4 (3.1) 0.159 Employment 5 (3.5) 2 (1.6) 0.326 Other 25 (17.4) 23 (18.1) 0.872 1 3 Supportive Care in Cancer (2023) 31:78 Page 5 of 9 78 Safety concerns related to COVID‑19 Barriers to resources and telemedicine Overall, the top concerns related to COVID-19 Urban-based providers reported significantly higher reported were similar between the urban- and subur- observed increase of barriers regarding access to prescrip- ban-/rural-based providers (Table  3). The most com- tions (29.9% vs. 16.5%, respectively, X = 6.64, p = 0.010). mon concern was patient safety (81.9%, 85.8%) fol- Additionally, urban providers reported higher observed lowed by treatment delays (62.5%, 66.9%), healthcare increase of transportation barriers (74.3%) compared to their provider mental health (55.6%, 58.3%), and personal suburban/rural counterparts (68.5%, p = 0.178). Suburban-/ family safety (51.4%, 55.9%) among urban and sub- rural-based providers reported higher observed increase of urban-/rural-based providers, respectively. Signifi - barriers among older adults accessing food (33.9%) and car- cant differences were observed by location for two egiver availability (66.1%) compared to their urban coun- 2 2 safety concerns: supply of PPE and patient mental terparts (31.3% and 62.5%, X = 2.09, p = 0.70; X = 0.39, health. Suburban-/r ural-based providers repor ted sig- p = 0.53, respectively). nificantly higher concerns about the supply of PPE There were no significant differences by provider loca- (62.2%) compared to urban-based providers (49.3%) tion in reported increase of perceived barriers to using (X = 4.54, p = 0.022). Lastly, urban-based providers telemedicine with older adults with cancer (Table 4). The reported significantly higher concerns about patient most reported perceived barriers were patient access (e.g., mental health (55.6%) than suburban-/rural-based pro- no smart phone, internet access) (91%, 92.1%), patient not viders (42.5%) (X = 4.59, p = 0.032). being tech savvy (89.6%, 92.1%), and patient perception Table 3 Top 5 concerns related Concerns Urban Suburban/rural Chi- to COVID-19 reported by n (%) n (%) square urban- and suburban-based p-value providers Patient safety 118 (81.9) 109 (85.8) 0.413 Treatment delay 90 (62.5) 85 (66.9) 0.447 Healthcare provider mental health 80 (55.6) 74 (58.3) 0.653 Patient mental health 80 (55.6) 54 (42.5) 0.032 My family safety 74 (51.4) 71 (55.9) 0.457 Personal safety 72 (50.0) 60 (52.8) 0.651 Supply of personal protective equipment 71 (49.3) 79 (62.2) 0.022 Patient mortality 67 (46.5) 47 (37.0) 0.113 Family of patient safety 24 (16.7) 23 (18.1) 0.754 Research delays 20 (13.9) 10 (7.9) 0.115 Clinical trial accrual 5 (3.5) 4 (3.1) 0.882 Table 4 Providers’ reported Variable Urban Suburban/rural Chi- barriers to using telehealth with n (%) n (%) square older adults with cancer p-value Patient access (e.g., no smart phone or internet 131 (91.0) 117 (92.1) 0.734 access) Patient not tech savvy 129 (89.6) 117 (92.1) 0.470 Patient perception issues 58 (40.3) 63 (49.6) 0.123 Program/institution infrastructure 43 (29.9) 37 (29.1) 0.896 Healthcare worker technology challenges 35 (24.3) 40 (31.5) 0.187 Healthcare worker home-work issues 23 (16.0) 23 (18.1) 0.640 Healthcare worker preference/policy 19 (13.2) 12 (9.4) 0.334 Uncertainty of reimbursement 17 (11.8) 16 (12.6) 0.842 Other barriers 9 (6.3) 9 (7.1) 0.811 No barriers 4 (2.8) 0 (0) 0.058 1 3 78 Page 6 of 9 Supportive Care in Cancer (2023) 31:78 issues of telemedicine (40.3%, 49.6%) among urban- and safety. Significant differences were observed regarding suburban-/rural-based providers, respectively. patient mental health (higher in urban-based providers) and supply of PPE (higher in suburban-/rural-based providers). These differences may be attributed to limited resources by Discussion location. COVID-19 surged in urban areas with limited men- tal healthcare support (both informal and formal) despite This study examined whether healthcare providers’ provi- increased demand during the data collection period. Tel- sion of as well as barriers to care for older adults with cancer emedicine challenges at that period may have also negatively differed between urban and suburban/rural settings. Signifi- impacted patient mental health [46–48]. At the same time, cant differences were found between urban and suburban/ the need for PPE was concentrated and subsequently pri- rural providers regarding their considerations for prioritizing oritized to those areas of surge, away from suburban/rural treatment for different age groups of patients with cancer; areas, leaving these providers with less PPE than the urban- urban-based providers were more likely to prioritize treat- based providers [49, 50]. ment for younger patients than older patients. This result is Barriers to using telemedicine were commonly experi- most likely due to the timing of the survey, April 2020, when enced by both urban and suburban/rural providers. This find - major urban centers such as New York City were experienc- ing was expected and understandable given the sudden pro- ing high numbers of COVID-19 cases. In later months, cases liferation of telemedicine among adults with cancer. The use surged in suburban and rural settings [39]. Contrary to the of telemedicine by some estimates grew 30-fold in the USA current study’s findings regarding treatment prioritization and almost 100-fold in the Medicare population in the sec- in urban settings, McGuire and colleagues argued that, in ond quarter of 2020 compared to before the pandemic [51, suburban/rural areas, patients may be more vulnerable to 52]. Before COVID-19, research found that older adults are the economic and health impacts of a pandemic [40]. They more receptive to technology use than was typically assumed posited that rural healthcare providers are not only fewer [53–55]. For example, over two-thirds of older adults use in number than their urban counterparts, but also work the internet daily and more than half have home broadband with fewer resources, less public transportation, and deliv- service [56]. However, as evidenced by this study and oth- ery options. Another potential reason for the difference in ers, older adults using technology may have barriers to tel- treatment prioritization by provider location may be related emedicine use, including internet and device access, design to the ageist approach that older adults with cancer should challenges, privacy and trust concerns, and cost [57–60]. For not receive equal treatment [15, 41, 42]. Previous studies example, Lam and colleagues found many older adults may have found that the COVID-19 pandemic has accentuated be unable to take part in health-related video visits because the exclusion and prejudice against older adults, warrant- of disabilities or inexperience with technology [60]. Again, ing immediate intervention and education [15, 41, 43, 44]. the timing of this survey may have influenced the reported This ageist perspective observed in the current study may barriers regarding telemedicine. In Spring 2020, the roll-out have emerged in part by the lack of written guidelines for of telemedicine was rapidly implemented to ensure adequate the management of older adults with cancer experienced by continuity of care while minimizing exposure to COVID- more than half of the rural- and suburban-based providers. 19. As telemedicine care becomes more widely used, it An additional possibility is the perception that older adults provides an important opportunity to expand telemedicine are more likely to have comorbidities or be frail and, hence, care to older, rural patients who live a greater distance from have increased risk for cancer treatment toxicity during tertiary medical centers, or to those older adults who may COVID-19 [45]. The current study’s findings support this have transportation or mobility limitations. Regardless of notion; urban respondents considered comorbidities and life location, modifications to telemedicine geriatric assessment expectancy (77%, 48%) at significantly higher prevalence as well as video visits [61] are important for promoting posi- than their suburban/rural counterparts (66%, 32%, respec- tive patient outcomes and patient-provider relationships, tively). Additional information about the provider’s patient facilitating clear communication, and observing non-verbal populations (e.g., median age, cancer stage) and their insti- communication [62–65]. tution’s response to COVID-19 (e.g., guidelines, hospital strain) as well as their experience (e.g., geriatric specializa- Limitations tions, trainings) would provide context for better understand- ing of the inclinations to prioritize treatment for different age The first limitation was that suburban and rural provider’s groups of patients with cancer. responses were combined to facilitate adequate sample Provider concerns regarding COVID-19 were similar size compared to the sample size of urban-based providers. regardless of provider location. The most reported concerns There could be differences between the two settings such were patient safety, treatment delays, and personal/family as resources and the impact of COVID-19 at the time of 1 3 Supportive Care in Cancer (2023) 31:78 Page 7 of 9 78 Data Availability Due to its proprietary nature, supporting data cannot the survey. In addition, there was an uneven distribution of be made openly available. healthcare providers (MDs and APPs versus social workers) based on location, which may skew the findings to a psy - Declarations chosocial lens rather than a treatment decision-making lens. Similarly, significantly more suburban/rural providers than Ethics approval The study was determined exempt by the University of Cincinnati Institutional Review Board as no identifying information urban providers were US-based, which can bias compari- was included in the collected data. sons between urban and suburban/rural provider responses. Lastly, several of the survey items asked explicitly about Consent to participate Electronic consent was received by participants caring for older adults. Therefore, respondents who did not prior to questionnaire completion. primarily care for older adults were asked to answer specifi- Consent for publication Participants were informed that the question- cally about this age group. This focus on older adults with naire results would be used for publications and provided their consent. cancer may skew the findings away from experiences related to the general population of patients with cancer. Conflict of interest The authors declare no competing interests. Conclusion References This study explored differences in urban and suburban/rural settings in the care provision of as well as barriers to can- 1. Broom A, Kenny K, Page A, Cort N, Lipp ES, Tan AC et  al cer care for older adults during COVID-19. 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JAMA Intern Med 180(10):1386–1389 author(s) or other rightsholder(s); author self-archiving of the accepted 60. Lam K, Lu AD, Shi Y, Covinsky KE (2020) Assessing telemedi- manuscript version of this article is solely governed by the terms of cine unreadiness among older adults in the United States during such publishing agreement and applicable law. the COVID-19 pandemic. JAMA Intern Med 180(10):1389–1391 Authors and Affiliations 1 2 3 4 5 Janell L. Pisegna  · Karlynn BrintzenhofeSzoc  · Armin Shahrokni  · Beverly Canin  · Elana Plotkin  · 5 6 7 8 9 Leigh M. Boehmer  · Leana Chien  · Mariuxi Viteri Malone  · Amy R. MacKenzie  · Jessica L. Krok‑Schoen Janell L. Pisegna System, University of Colorado Anschutz Medical Campus, janell.pisegna@cuanschutz.edu Aurora, CO, USA Karlynn BrintzenhofeSzoc Kent School of Social Work, University of Louisville, karlynn.brintzenhofeszoc@louisville.edu Louisville, KY, USA Armin Shahrokni Department of Medicine, Gastrointestinal Oncology shahroka@mskcc.org and Geriatrics Services, Memorial Sloan Kettering Cancer Center, New York, NY, USA Beverly Canin caninbeverly@gmail.com Cancer and Aging Research Group, Duarte, CA, USA Elana Plotkin Provider Education Programs, Association of Community EPlotkin@accc-cancer.org Cancer Centers, Rockville, Maryland, USA Leigh M. Boehmer City of Hope Comprehensive Cancer Center, Duarte, CA, lboehmer@accc-cancer.org USA Leana Chien Division of Hematology, Florida Cancer Specialists lchien@coh.org and Research Institute, Venice, FL, USA Mariuxi Viteri Malone Division of Hematology, Thomas Jefferson University, mariux.viteri@gmail.com Philadelphia, PA, USA Amy R. MacKenzie School of Health and Rehabilitation Sciences, College Amy.Mackenzie@jefferson.edu of Medicine, The Ohio State University, 453 W. 10Th Ave., Columbus, OH 43210, USA Physical Therapy Program, Geriatric Research Education and Clinical Center VA Eastern Colorado Healthcare 1 3

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Supportive Care in CancerPubmed Central

Published: Dec 23, 2022

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