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Loneliness, social isolation, and social support in older adults with active cancer during the COVID-19 pandemic

Open AccessPublished:August 17, 2022DOI:https://doi.org/10.1016/j.jgo.2022.08.003

      Abstract

      Introduction

      The COVID-19 pandemic has had a considerable impact on mental health. The social distancing and stay-at-home orders have likely also impacted loneliness, social isolation, and social support. Older adults, particularly those with comorbidities such as cancer, have a greater potential to be impacted. Here we assessed loneliness, social isolation, and social support in older adults undergoing active cancer treatment during the pandemic.

      Materials and methods

      A mixed methods study in which quantitative data and qualitative response items were collected in parallel was conducted in 100 older adults with cancer. Participants completed a survey by telephone with a series of validated questionnaires to assess the domains of loneliness, social isolation, and social support as well as several open-ended questions. Baseline demographics and geriatric assessments were summarized using descriptive statistics. Bivariate associations between social isolation and loneliness and social support and loneliness were described using Spearman correlation coefficients. Conventional content analysis was performed on the open-ended questions.

      Results

      In a population of older adults with cancer, 3% were noted to be severely lonely, although 27% percent screened positive as having at least one indicator of loneliness by the University of California, Los Angeles (UCLA) Three Item Loneliness Scale. There was a significant positive correlation between loneliness and social isolation (r = +0.52, p < 0.05) as well as significant negative correlation between loneliness and social support (r = −0.49, p < 0.05). There was also a significant negative correlation between loneliness and emotional support (r = −0.43, p < 0.05). There was no significant association between loneliness and markers of geriatric impairments, including comorbidities, G8 score or cognition.

      Discussion

      Reassuringly, in this cohort we found relatively low rates of loneliness and social isolation and high rates of social support. Consistent with prior studies, loneliness, social isolation, and social support were found to be interrelated domains; however, they were not significantly associated with markers of geriatric impairments. Future studies are needed to study if cancer diagnosis and treatment may mediate changes in loneliness, social isolation, and social support in the context of the pandemic as well as beyond.

      Keywords

      1. Introduction

      The COVID-19 pandemic and its attendant mitigation strategies, including stay-at-home orders and social distancing, have made consideration of the health impact of social connection increasingly relevant [
      • Wu B.
      Social isolation and loneliness among older adults in the context of COVID-19: a global challenge.
      ,
      • Sepúlveda-Loyola W.
      • et al.
      Impact of social isolation due to COVID-19 on Health in older people: mental and physical effects and recommendations.
      ]. Loneliness, social isolation, and social support are interrelated but distinct concepts that require consideration in this context. While the term loneliness often refers to the subjective feeling of being alone, social isolation refers to the absence of interpersonal interactions [
      • Larose S.
      • Guay F.
      • Boivin M.
      Attachment, social support, and loneliness in young adulthood: a test of two models.
      ,
      • Valtorta N.
      • Hanratty B.
      Loneliness, isolation and the health of older adults: do we need a new research agenda?.
      ]. Social support has a variety of definitions, including both quantitative and qualitative dimensions [
      • Pearson J.E.
      The definition and measurement of Social support.
      ]. Qualitative social support refers to the perceived meaning and values people ascribe to their relationships [
      • Nguyen A.W.
      • et al.
      Social support from family and friends and subjective well-being of Older African Americans.
      ]. Quantitative social support focuses on social network, including the length and complexity of relationships [
      • Kaplan B.H.
      • Cassel J.C.
      • Gore S.
      Social support and health.
      ]. These terms have been shown to overlap, and each has important implications for older adults [
      • Donovan N.J.
      • Blazer D.
      Social isolation and loneliness in older adults: review and commentary of a national academies report.
      ] and individuals with cancer [
      • Importance of Social Support in Cancer Patients
      ].
      Models of loneliness have theorized that the perceived sense of social isolation results in feeling unsafe, which leads to a hypervigilance of additional social threats [
      • Cacioppo J.T.
      • et al.
      Loneliness within a nomological net: an evolutionary perspective.
      ]. Consequently, loneliness has important impact on both mental and physical health. Loneliness is a specific risk factor for depressive symptoms, as well as for functional decline, morbidity and mortality [
      • Hawkley L.C.
      • Cacioppo J.T.
      Loneliness matters: a theoretical and empirical review of consequences and mechanisms.
      ,
      • Cacioppo J.T.
      • et al.
      Loneliness as a specific risk factor for depressive symptoms: cross-sectional and longitudinal analyses.
      ,
      • Perissinotto C.M.
      • Stijacic Cenzer I.
      • Covinsky K.E.
      Loneliness in older persons: a predictor of functional decline and death.
      ]. Similar to loneliness, social isolation has many overlapping effects on health [
      • Nicholson N.R.
      A review of social isolation: an important but underassessed condition in older adults.
      ]. Social isolation has clear impact on physical health and is associated with poorer cognitive functioning, coronary heart disease, and all-cause mortality [
      • DiNapoli E.A.
      • Wu B.
      • Scogin F.
      Social isolation and cognitive function in Appalachian older adults.
      ,
      • Eng P.M.
      • et al.
      Social ties and change in social ties in relation to subsequent total and cause-specific mortality and coronary heart disease incidence in men.
      ,
      • Fratiglioni L.
      • et al.
      Influence of social network on occurrence of dementia: a community-based longitudinal study.
      ,
      • Mistry R.
      • et al.
      Social isolation predicts re-hospitalization in a group of older American veterans enrolled in the UPBEAT program.
      ]. Socially isolated individuals with cancer are more likely to be adversely affected by their cancer diagnosis [
      • Michael Y.L.
      • et al.
      Social networks and health-related quality of life in breast cancer survivors: a prospective study.
      ] and have inferior survival [
      • Moore S.
      • et al.
      Social isolation: impact on treatment and survival in patients with advanced cancer.
      ,
      • Kroenke C.H.
      • et al.
      Social networks, social support, and survival after breast cancer diagnosis.
      ]. Furthermore, amount of social support has important implications for individuals with cancer [
      • Usta Y.Y.
      Importance of social support in cancer patients.
      ] as higher levels of social support are associated with decreased mortalty [
      • Pinquart M.
      • Duberstein P.R.
      Associations of social networks with cancer mortality: a meta-analysis.
      ].
      The novel coronavirus (COVID-19) has resulted in over 840,286 deaths in the United States alone as of January 2022 [
      • Prevention, C.F.D.C.A
      United States COVID-19 Cases, Deaths, and Laboratory Testing (NAATs) by State, Territory, and Jurisdiction.
      ]. While social isolation during the COVID-19 pandemic has been particularly emphasized for vulnerable populations such as older adults, the recommendation for physical distancing with resultant social isolation may be especially distressing for people living with cancer who rely on social support [
      • Al-Shamsi H.O.
      • et al.
      A practical approach to the management of cancer patients during the novel coronavirus disease 2019 (COVID-19) pandemic: an international collaborative group.
      ,
      • Ford M.B.
      Social distancing during the COVID-19 pandemic as a predictor of daily psychological, social, and health-related outcomes.
      ]. Older adults, who traditionally have less familiarity with technology, may be further isolated [
      • Vaportzis E.
      • Giatsi Clausen M.
      • Gow A.J.
      Older adults perceptions of technology and barriers to interacting with tablet computers: a focus group study.
      ]. The early studies of the effects of the pandemic on social isolation and loneliness are limited, with somewhat mixed results. While upwards of 56% of people over the age of 50 have reported feeling isolated from others, compared to 27% of people in a similar poll in 2018 [
      ], other studies have found that older adults reported lower rates of loneliness compared to younger adults and no change compared to prior rates [
      • Groarke J.M.
      • et al.
      Loneliness in the UK during the COVID-19 pandemic: cross-sectional results from the COVID-19 psychological wellbeing study.
      ,
      • Peng S.
      • Roth A.R.
      Social isolation and loneliness before and during the COVID-19 pandemic: a longitudinal study of U.S. Adults Older than 50.
      ]. Studies of the effects of the pandemic in patients with cancer have shown high levels of stress and symptom burden [
      • Miaskowski C.
      • et al.
      Stress and symptom burden in oncology patients during the COVID-19 pandemic.
      ]. A study of patients with cancer found that over half of participants were lonely and reported higher levels of social isolation; however, this was more pronounced in the younger population [

      Miaskowski, C., et al., Loneliness and symptom burden in oncology patients during the COVID-19 pandemic. Cancer.

      ]. Another study in older breast cancer survivors found changes in loneliness during the pandemic similar to those reported by individuals without cancer [
      • Rentscher K.E.
      • et al.
      Loneliness and mental health during the COVID-19 pandemic in older breast cancer survivors and noncancer controls.
      ].
      Few studies have examined the implications of the COVID-19 pandemic on feelings of loneliness, social isolation, and social support in older adults undergoing active cancer treatment. Here we assessed loneliness, social isolation, and social support in older adults with cancer during the pandemic.

      2. Materials and Methods

      We performed a mixed methods study in which quantitative data and qualitative response items were collected in parallel [
      • Shorten A.
      • Smith J.
      Mixed methods research: expanding the evidence base.
      ]. Informed consent was obtained from patients age 65 or older with a biopsy-proven malignancy who were receiving active systemic therapy, such as intravenous chemotherapy or oral medications, and anticipated to continue to receive care at Siteman Cancer Center (SCC). Patients on active surveillance alone or in survivorship clinics were excluded. Potential study candidates were identified from the patients who were seeking initial consultation or continued treatment with a medical oncologist at the SCC. Patients were enrolled onto the study until the recruitment goal of 100 patients was met.
      Potential participants were screened from the solid tumor oncology clinic schedule at SCC and contacted by telephone by research team members. Following verbal consent, basic demographic information was collected from the medical record at the time of patient consent, including age/sex, race/ethnicity, cancer diagnosis/staging, description of treatment, and Charlson comorbidity index. Cancer diagnosis was included in the Charlson comorbidity index calculations for all participants. Participants then completed a mixed methods survey by telephone with a series of validated questionnaires to assess the domains of loneliness, social isolation, and social support as well as several open-ended questions. Measures included the G8 geriatric screening tool [
      • Bellera C.A.
      • et al.
      Screening older cancer patients: first evaluation of the G-8 geriatric screening tool.
      ], Patient-Reported Outcomes Measurement Information System (PROMIS) Bank v2.0 Emotional Support Short Form 4a, PROMIS Bank v2.0-Social Isolation Short Form 8a [
      • Ader D.N.
      Developing the patient-reported outcomes measurement information system (PROMIS).
      ], University of California, Los Angeles (UCLA) loneliness scale [
      • Russell D.
      • Peplau L.A.
      • Ferguson M.L.
      Developing a measure of loneliness.
      ], the Medical Outcomes Study (MOS) social support survey [
      • Sherbourne C.D.
      • Stewart A.L.
      The MOS social support survey.
      ], and the Short Blessed Test [
      • Katzman R.
      • et al.
      Validation of a short orientation-memory-concentration test of cognitive impairment.
      ]. These measures were not modified.
      Patients were then asked a short series of open-ended questions at the end of the telephone interview to better understand the impact of the COVID-19 pandemic on loneliness. Responses were summarized and recorded by the research coordinator.
      To account for the dynamic status of the COVID-19 pandemic, the average seven-day new confirmed cases and average test positivity rate for St. Louis region at the time of the telephone interview and in-person assessment, as publicly reported (https://www.stlouis-mo.gov/covid-19/data/) were recorded for each participant.
      The study was approved by the Washington University School of Medicine Human Studies Committee.

      2.1 Measures

      2.1.1 Loneliness

      Loneliness was defined based on the UCLA Loneliness Scale long form [
      • Russell D.
      • Peplau L.A.
      • Ferguson M.L.
      Developing a measure of loneliness.
      ] as well as UCLA Three Item Loneliness Scale [
      • Hughes M.E.
      • et al.
      A short scale for measuring loneliness in large surveys: results from two population-based studies.
      ]. Using the original UCLA Loneliness Scale, scores >30 were defined as severe loneliness. Using the Three Item UCLA Loneliness Scale, loneliness was categorized in two ways [

      Kotwal, A.A., et al., The epidemiology of social isolation and loneliness among older adults during the last years of life. J Am Geriatr Soc.

      ]. “Any loneliness” was defined as 1+ points on the scale and “frequently lonely” was defined as 4+ points on the scale.

      2.1.1.1 PROMIS Bank Emotional Support Short Form 4a – Version 2

      The PROMIS Emotional Support bank evaluates relationships and perceived feelings of being valued. The T-score was calculated, which rescaled the raw score into a standardized score with a mean of 50 in a general US reference population and a standard deviation (SD) of 10 [
      • Ader D.N.
      Developing the patient-reported outcomes measurement information system (PROMIS).
      ]. A higher PROMIS T-score represents more of the concept being measured. Higher scores represent better emotional support.

      2.1.1.2 PROMIS Bank Social Isolation Short Form 8a – Version 2

      The PROMIS Social Isolation bank evaluates perceived feelings of being excluded or disconnected from other individuals. A T-score was also calculated as above and a higher score indicates higher levels of social isolation [
      • Carlozzi N.E.
      • et al.
      Understanding health-related quality of life of caregivers of civilians and service members/veterans with traumatic brain injury: establishing the reliability and validity of PROMIS social health measures.
      ].

      2.1.1.3 MOS Social Support Survey

      MOS measures the availability of support in several domains. For this study, emotional/informational (eight questions) and tangible (four questions) support domains were used. The mean item response for each subscale was calculated and then scores were transformed to have a possible range of 0–100, with higher scores indicating more support [
      • Sherbourne C.D.
      • Stewart A.L.
      The MOS social support survey.
      ].

      2.2 Statistical Analysis

      The sample size of this pilot study was determined based on that anticipated recruitment feasible during the study period and was 100 older adults with cancer. It was estimated that a sample size of 100 would allow for an estimation of the true mean score on the UCLA loneliness scale with a margin of error of ±9.8 (95% confidence interval [CI]) [
      • Russell D.
      • Peplau L.A.
      • Ferguson M.L.
      Developing a measure of loneliness.
      ].
      Baseline demographics and geriatric assessments were summarized using descriptive statistics. Bivariate associations between social isolation and loneliness and social support and loneliness were described using Pearson correlation coefficients. Exploratory analysis of the relationship between social isolation, loneliness, social support, and other variables including sex, cancer types, stage, treatment type, education, marital status, living situation, employment, income, and average COVID cases was performed using non-parametric Kruskal-Wallis rank-sum test to compare the average T-scores among the subgroups defined by these variables such as sex, education, etc. Partial correlation coefficients for loneliness versus social isolation or social support were also calculated after adjusting demographic and clinical variables. All analyses were two-sided and significance was set at a p-value of 0.05. Statistical analyses were performed using SAS 9.4 (SAS Institutes, Cary NC).

      2.3 Content Analysis

      Conventional content analysis was performed on the open-ended questions [
      • Hsieh H.-F.
      • Shannon S.E.
      Three approaches to qualitative content analysis.
      ]. The patient responses were reviewed and codes were created based on unique responses which were then sorted into groups. A descriptive analysis of these groups was then performed.

      3. Results

      From March 2021 to July 2021, 100 patients were enrolled. Baseline demographic values are presented in Table 1. The mean age of participants was 74.28 years. The majority of participants were White (86%) females (58%) receiving oral therapy (59%). The majority of participants were married (55%) and living with a spouse (54%). Thirty-one percent of participants lived alone, 21% were divorced and 17% were widowed. The majority of patients were retired (75%) and had either an advanced degree (34%) or college degree (21%). The majority of participants reported a yearly household income of $50,000 or greater (57%). The majority of participants had a diagnosis of breast (44%) or prostate cancer (23%) and were stage IV (56%). The average seven-day new confirmed COVID-19 cases in the city of Saint Louis during the time of the study was 23.49. The average test positivity rate in the city of Saint Louis was 5.59%.
      Table 1Demographics.
      VariableNumber of patients (N = 100)
      AgeMean +/− standard deviation74.28 ± 5.58
      SexMale42
      Female58
      RaceWhite86
      African American14
      EthnicityHispanic1
      Non-Hispanic99
      Other0
      Current Treatment
      Sum >100 due to patients being on more than one type of therapy concurrently.
      IV Chemotherapy24
      Oral Therapy59
      Immunotherapy13
      Other, including clinical trial29
      Education LevelGrades 1–80
      Grades 9–113
      High school or GED18
      Some college15
      Some junior college7
      College Degree21
      Post-college work2
      Advanced Degree34
      Marital StatusMarried55
      Divorced21
      Widowed17
      Single7
      Living SituationSpouse54
      Parents/Parents-in-law1
      Alone31
      Children, age ≤ 181
      Children, age > 187
      Other5
      Employment StatusEmployed >32 h/week9
      Employed <32 h/week8
      Homemaker1
      Medical leave1
      Disabled0
      Unemployed2
      Retired75
      Other4
      Yearly HouseholdLess than $50003
      Income$5000–$19,9999
      $20,000–$49,99924
      $50,000–$99,99925
      $100,000–$149,99914
      Over $150,00018
      Prefer not to answer7
      Cancer TypesBreast Cancer44
      Prostate Cancer23
      Others33
      Cancer StageI29
      II/III14
      IV56
      low asterisk Sum >100 due to patients being on more than one type of therapy concurrently.
      Results of the geriatric assessment, as well as measures of loneliness, social isolation, and social support are presented in Table 2. The mean BMI for the cohort was 23.49 and the mean Charlson comorbidity index was 7.66. On the G-8 geriatric screening tool, 62% of patients scored ≤14, which is considered abnormal. Only 2% of patients scored >9 (abnormal) on the Short Blessed Test. On the UCLA Loneliness scale, 3% of participants scored >30, which is considered severely lonely. By the UCLA Three Item Loneliness Scale, 27% scored ≥1, indicating any loneliness. The mean T Score for the PROMIS Bank v2.0 Emotional Support Short Form 4a was 56.67 and the mean T score PROMIS Bank v2.0 Social Isolation Short Form 8a was 43.94. The mean MOS Social Support Score was 82.64.
      Table 2Outcome Variables in cohort of older adults on chemotherapy completing survey of loneliness and social isolation (N = 100).
      BMI (Mean, range)23.49 (17.54–55.17)
      G-8 geriatric screening tool
      > 1438
      ≤ 14 (abnormal)62
      Charlson comorbidity index (Mean, range)7.66 (4, 13)
      Short Blessed Test >9 (frequency, percent)2/100 (2%)
      UCLA Loneliness Scale
      ≤ 3097
      > 30 (severely lonely)3
      UCLA Three Item Loneliness Scale
      073
      ≥ 1 (any loneliness)27
      ≥ 4 (frequently lonely)3
      PROMIS Bank v2.0 Emotional Support Short Form 4a (T score Mean, range)56.67 (42.10–62.00)
      PROMIS Bank v2.0 Social Isolation Short Form 8a (T score Mean, range)43.94 (33.90–64.50)
      MOS Social Support Score (Mean, range)82.64 (0−100)
      BMI, body mass index; UCLA, University of California, Los Angeles; PROMIS, Patient-Reported Outcomes Measurement Information System; MOS, Medical Outcomes Study.
      All questionnaires showed very good internal consistency, with standardized Cronbach's alpha of 0.78, 0.87, 0.92, 0.95, and 0.72 for PROMIS Emotional Support, PROMIS Social Isolation, MOS Social Support, UCLA Long Form, and UCLA Short Form, respectively.
      There was a significant positive correlation between loneliness and social isolation (r = +0.52, p < 0.05) as well as significant negative correlation between loneliness and social support (r = −0.49, p < 0.05). There was also a significant negative correlation between loneliness and emotional support (r = −0.43, p < 0.05). These correlations were significant using both the UCLA long form as well as short form.
      There was no significant association between loneliness and markers of geriatric impairments, including comorbidities, G8 score, or cognition. Similarly, there was no significant association between social isolation, social support, or emotional support and markers of geriatric impairments, including comorbidities, G8 score, or cognition.
      The association between loneliness (Fig. 1), social isolation (Fig. 2), emotional support (Fig. 3) and social support (Fig. 4) and multiple demographic variables, including sex, income status, marital status, education level, employment status, living situation, cancer stage, cancer type, and treatment were then analyzed. There was a significant (p < 0.05) association between loneliness and sex, income status, marital status, and living situation. Higher rates of loneliness were associated with being female, annual household income <$50,000 per year, divorced individuals, and individuals living alone or with an individual other than a spouse. There was a significant (p < 0.05) association between social isolation and sex and income status. Higher rates of social isolation were associated with being female with an annual household income <$50,000 per year. There was a significant (p < 0.05) association between emotional support and treatment type. Lower rates of emotional support were associated with patients receiving oral therapy and immunotherapy. There was a significant (p < 0.05) association between social support and living situation and treatment type. Lower rates of social support were associated with living alone and with patients receiving oral therapy and immunotherapy.
      Fig. 1
      Fig. 1Association between loneliness and demographic variables in cohort of older adults on chemotherapy completing survey of loneliness and social isolation (N = 100).
      Fig. 2
      Fig. 2Association between social isolation and demographic variables in cohort of older adults on chemotherapy completing survey of loneliness and social isolation (N = 100).
      Fig. 3
      Fig. 3Association between emotional support and demographic variables in cohort of older adults on chemotherapy completing survey of loneliness and social isolation (N = 100).
      Fig. 4
      Fig. 4Association between social support and demographic variables in cohort of older adults on chemotherapy completing survey of loneliness and social isolation (N = 100).
      There was no significant association between loneliness, social isolation, emotional support, and social support and daily average number of COVID-19 cases. After adjusting these demographic variables, the conclusion remained unchanged, with a positive correlation between loneliness and social isolation (r = +0.45, p < 0.05), and a negative correlation between loneliness and social support (r = −0.44, p < 0.05), as well as between loneliness and emotional support (r = −0.40, p < 0.05).

      3.1 Open Ended Questions

      3.1.1 How has COVID-19 pandemic affected you?

      On review of responses, three distinct themes were identified: the COVID-19 pandemic did not affect participants, participants found ways to adapt to the pandemic, and/or participants were affected by the pandemic. Representative responses of these themes are presented in Table 3. The majority of patients (N = 57) discussed how the pandemic has affected them, with the most common ways including physical isolation (N = 32) and change of routines (N = 29). One participant described “It was awful. It was horrible. I have cancer and low blood counts so I was very careful and in isolation for a whole year. I missed two years of my granddaughter's life. I was in remission, but I got diagnosed with cancer right after I got the COVID-19 vaccine, so it has been really hard.”
      Table 3Representative responses to the open-ended question: How has COVID-19 pandemic affected you?
      No effect (N = 41)Adapted (N = 19)Affected (N = 57)
      Continued to have support system of family, friends, etc. (15)Found solutions (3)Changed routines (stopped volunteering, traveling) (29)
      Previously accustomed to being alone (5)Used technology for interacting with others (7)Physical isolation (stayed at home) (32)
      Participated in indoor hobbies (reading, cooking) (5)Loneliness (1)
      Interacted outdoors (5)Made cancer diagnosis more difficult (3)
      Interacted in “pods” (2)Mental health (depression, anxiety, fear) (6)
      A large number of respondents did state that the pandemic had not affected them (N = 41), most commonly citing that they continued to have support from friends and/or family (N = 15). A subset of patients described ways they adapted to the pandemic (N = 19), including using technology to interact with other (N = 7), interacting outdoors (N = 5) and in “pods” (N = 2), and participating in hobbies (N = 5).
      Have you or do you plan to receive a vaccination against the COVID-19 pandemic when available? If yes, how do you perceive this has changed or will change your feelings of loneliness and social isolation?
      The overwhelming majority (95%) of patients had received (N = 88) or planned to receive (N = 7) their COVID-19 vaccination. Of those, 26.3% (N = 25) felt that the vaccination would not change their feelings of loneliness or social isolation. Twenty-seven patients (28.4%) responded that the vaccination did change their perceptions by allowing them to socialize, resume previous activities, and travel. One participant responded, “It absolutely changed my feelings. A great weight was lifted.”
      Based upon all the things we discussed today, is there anything else you would like to add?
      A theme that emerged from the final open-ended question was one of gratitude, with fourteen participants answering that they felt grateful for the support system in their life. One participant noted “The questions make me feel grateful for what I have with my husband and other people in my bubble.” Another eight patients expressed appreciation for being asked about loneliness and social isolation. Other patients offered advice, “Don't sit in it! People need to try to create something positive.”

      4. Discussion

      We conducted a cross-sectional mixed methods pilot study to assess loneliness, social isolation, and social support in older adults on active treatment for cancer during the COVID-19 pandemic. Reassuringly, in this cohort we found relatively low rates of loneliness and social isolation and high rates of social support. Only a small population in the study, 3%, were noted to be severely lonely although 27% percent screened positive as having at least one indicator loneliness by the UCLA short form. This is in contrast with another study in patients with cancer during the COVID-19 pandemic, which found 53% of patients with cancer were classified as lonely; however, this was in a younger patient population [
      • Miaskowski C.
      • et al.
      Stress and symptom burden in oncology patients during the COVID-19 pandemic.
      ]. Multiple studies in a general population also found age to be a risk factor for loneliness, with younger adults exhibiting higher rates of loneliness [
      • Groarke J.M.
      • et al.
      Loneliness in the UK during the COVID-19 pandemic: cross-sectional results from the COVID-19 psychological wellbeing study.
      ,
      • Losada-Baltar A.
      • et al.
      “We are staying at home.” Association of self-perceptions of aging, personal and family resources, and loneliness with psychological distress during the lock-down period of COVID-19.
      ,
      • Bu F.
      • Steptoe A.
      • Fancourt D.
      Loneliness during strict lockdown: trajectories and predictors during the COVID-19 pandemic in 38,217 adults in the UK.
      ,
      • Li L.Z.
      • Wang S.
      Prevalence and predictors of general psychiatric disorders and loneliness during COVID-19 in the United Kingdom.
      ,
      • Luchetti M.
      • et al.
      The trajectory of loneliness in response to COVID-19.
      ]. Larger pre-pandemic studies have shown that age is a major risk factor for loneliness and may decline as individuals grow older [
      • Shovestul B.
      • et al.
      Risk factors for loneliness: the high relative importance of age versus other factors.
      ]. Younger individuals may report increased levels of perceived social isolation as the pandemic may have disrupted more social activities such as travel and education. Older adults who are retired and accustomed to staying at home, in contrast, may have had less disruption to their schedules. Additionally, another study revealed older adults exhibited resilience and used technology to protect themselves from loneliness during the pandemic [
      • Peng S.
      • Roth A.R.
      Social isolation and loneliness before and during the COVID-19 pandemic: a longitudinal study of U.S. Adults Older than 50.
      ].
      Females were more likely to be lonely in our patient population. Previous studies regarding sex and loneliness have been mixed, with some studies revealing females are more lonely [
      • Borys S.
      • Perlman D.
      Gender Differences in Loneliness.
      ,
      • Dahlberg L.
      • Agahi N.
      • Lennartsson C.
      Lonelier than ever? Loneliness of older people over two decades.
      ,
      • Beutel M.E.
      • et al.
      Loneliness in the general population: prevalence, determinants and relations to mental health.
      ] and others that men are more lonely [
      • Barreto M.
      • et al.
      Loneliness around the world: age, gender, and cultural differences in loneliness.
      ,
      • Hawkley L.C.
      • et al.
      From social structural factors to perceptions of relationship quality and Loneliness: the Chicago health, aging, and social relations study.
      ]. A recent large meta-analysis revealed no significant sex differences [
      • Maes M.
      • et al.
      Gender differences in Loneliness across the lifespan: a meta-analysis.
      ]. Married individuals were found to be the least lonely, consistent with previous studies [
      • Stack S.
      Marriage, family and loneliness: a cross-national study.
      ,
      • Fokkema T.
      • De Jong Gierveld J.
      • Dykstra P.A.
      Cross-national differences in older adult loneliness.
      ,
      • Umberson D.
      • Williams K.
      Marital quality, health, and aging: gender equity?.
      ]. Similarly, those living with a partner reported significantly lower rates of loneliness and higher social support, while those living alone or living with another relative or children reported similar rates of loneliness. Those reporting annual incomes <$50,000 had the highest rates of loneliness and social isolation, a finding that has also been shown in recent studies of loneliness during the COVID-19 pandemic [
      • McQuaid R.J.
      • et al.
      The burden of loneliness: implications of the social determinants of health during COVID-19.
      ,
      • Bu F.
      • Steptoe A.
      • Fancourt D.
      Who is lonely in lockdown? Cross-cohort analyses of predictors of loneliness before and during the COVID-19 pandemic.
      ].
      Levels of social support were similar to previous studies of patients with cancer prior to the pandemic [
      • Hurria A.
      • et al.
      Predicting chemotherapy toxicity in older adults with cancer: a prospective multicenter study.
      ,
      • Magnuson A.
      • et al.
      Development and validation of a risk tool for predicting severe toxicity in Older Adults receiving chemotherapy for early-stage breast Cancer.
      ]. This study found high levels of emotional support and lower levels of social isolation, which are calibrated to the US general population. While the PROMIS scores were developed in a general population and prior to the COVID-19 pandemic, a study of changes in the PROMIS Global Health during the pandemic in a general population only found modest and non-clinically meaningful decreases in global mental and physical health [
      • Lapin B.R.
      • et al.
      Evidence of stability in patient-reported Global Health during the COVID-19 pandemic.
      ]. It may be hypothesized that the levels of emotional support and lower levels of social isolation may be moderated by patients' cancer diagnoses and treatment. Patients with cancer may receive more emotional and social support from caregivers and have less social isolation as they require frequent interactions with the medical establishment. Similarly, a study of Americans 50 years or older during the COVID-19 pandemic found lower rates of social isolation in participants who had access to a healthcare provider and access to medications [
      • Peckham A.
      • et al.
      Aging through the time of COVID-19: a survey of self-reported healthcare access.
      ].
      Loneliness, however, was associated with lower rates of emotional support and higher rates of social isolation, as found with a recent study of patients with cancer during the COVID-19 pandemic [

      Miaskowski, C., et al., Loneliness and symptom burden in oncology patients during the COVID-19 pandemic. Cancer.

      ]. Higher rates of loneliness were also associated with less social support, which is similar to a previous meta-analysis in oncology patients [
      • Deckx L.
      • van den Akker M.
      • Buntinx F.
      Risk factors for loneliness in patients with cancer: a systematic literature review and meta-analysis.
      ].
      Loneliness, emotional support, social isolation, and social support were not significantly associated with markers of geriatric impairments used in this study, including comorbidities, G8 score, or cognition. This is in contrast with previous studies in which loneliness was associated with increased comorbidities and poorer functional status [

      Miaskowski, C., et al., Loneliness and symptom burden in oncology patients during the COVID-19 pandemic. Cancer.

      ,
      • Philip K.E.J.
      • et al.
      Social isolation, loneliness and physical performance in older-adults: fixed effects analyses of a cohort study.
      ]. This may be explained by the relatively low rates of loneliness in this cohort, but underscores the need to consider screening for loneliness rather than relying on the presence of other geriatric impairments as a marker for loneliness.
      The open-ended questions in our study added context to the quantitative data. Several important themes were identified in regards to how the pandemic affected patients. The majority of participants (N = 57) felt affected by the pandemic, including increased physical isolation (N = 32) and change of routines (N = 29). However, large numbers of participants felt the pandemic did not affect them (N = 41) and discussed ways they adapted (N = 19). Many participants also discussed gratitude for their support system. The open-ended responses add additional context to the findings of high levels of social and emotional support and lower levels of loneliness and social isolation.

      4.1 Strengths

      There are several strengths to this study. Unlike many studies which are conducted in patients with cancer on active surveillance, our study was conducted in older adults undergoing active treatment. This population was likely immunocompromised and vulnerable to the social distancing guidelines and restrictions during the COVID- 19 pandemic. Our study was also conducted over the telephone rather than by email, and therefore may have captured additional older adults who have lower proficiency with technology. The telephone nature of the survey also allowed for adherence to the social distancing guidelines and did not put participants at risk for COVID-19. The open-ended questions provided additional context and enriched the participant's responses.

      4.2 Limitations

      There are several limitations in this study. The study was a cross-sectional study and therefore we are unable to compare rates of loneliness, social isolation, and social support in this cohort during the COVID-19 pandemic to prior to the pandemic or assess for any changes in these domains. Furthermore, the cohort was comprised of largely White, educated individuals with high vaccination rates and therefore may not be generalizable to a larger population. The survey response rate was not recorded, so the representativeness of those who agreed to participate is not known. Furthermore, we did not survey similar individuals without cancer and therefore cannot assess if characteristics from the cohort are unique to patients with cancer or if there are other variables influencing the analysis. Our sample was derived from a population of patients seeking care at a tertiary care facility and thus represents individuals who are either geographically proximate or who have the resources and social support to travel to our institution; thus it is not representative of all older adults with cancer in the United States.

      4.3 Implications

      The effect of loneliness on mortality has been found to be comparable to other well-known risk factors such as obesity and cigarette smoking [
      • Holt-Lunstad J.
      • Smith T.B.
      • Layton J.B.
      Social relationships and mortality risk: a Meta-analytic review.
      ,
      • Penninx B.W.
      • et al.
      Effects of social support and personal coping resources on mortality in older age: the longitudinal aging study Amsterdam.
      ]. Loneliness has been associated with increased risk of coronary heart disease, hypertension, cognitive dysfunction, and poor sleep quality [
      • Cacioppo J.T.
      • Hawkley L.C.
      Perceived social isolation and cognition.
      ,
      • Jacobs J.M.
      • et al.
      Global sleep satisfaction of Older people: the Jerusalem cohort study.
      ,
      • Friedman E.M.
      • et al.
      Social relationships, sleep quality, and interleukin-6 in aging women.
      ,
      • Thurston R.C.
      • Kubzansky L.D.
      Women, loneliness, and incident coronary heart disease.
      ,
      • Hawkley L.C.
      • et al.
      Loneliness is a unique predictor of age-related differences in systolic blood pressure.
      ]. Loneliness among middle-aged men has been associated with an increased likelihood of cancer [
      • Kraav S.L.
      • et al.
      Loneliness and social isolation increase cancer incidence in a cohort of Finnish middle-aged men. A longitudinal study.
      ]. It may also have important implications for the treatment of cancer as it may upregulate inflammatory gene expression [
      • Cole S.W.
      • et al.
      Myeloid differentiation architecture of leukocyte transcriptome dynamics in perceived social isolation.
      ] and has been associated with impaired cellular immunity and decreased NK cell activity [
      • Kiecolt-Glaser J.K.
      • et al.
      Psychosocial modifiers of immunocompetence in medical students.
      ]. Similarly, socially isolated individuals are at higher risk for negative health behaviors such as heavy drinking, smoking, decreased physical activity, and poor nutrition [
      • Eng P.M.
      • et al.
      Social ties and change in social ties in relation to subsequent total and cause-specific mortality and coronary heart disease incidence in men.
      ,
      • Hanson B.S.
      • et al.
      Social support and quitting smoking for good. Is there an association? Results from the population study, “men born in 1914,” Malmö, Sweden.
      ,
      • Locher J.L.
      • et al.
      Social isolation, support, and capital and nutritional risk in an older sample: ethnic and gender differences.
      ,
      • Eriksen W.
      • Sandvik L.
      • Bruusgaard D.
      Social support and the smoking behaviour of parents with preschool children.
      ,
      • Broman C.L.
      Social relationships and health-related behavior.
      ]. The relationship between social isolation and mental health is not as well understood, with some studies reporting associations between social isolation and depression [
      • Dorfman R.A.
      • et al.
      Screening for depression among a well elderly population.
      ] while others not [
      • Schoevers R.A.
      • et al.
      Risk factors for depression in later life; results of a prospective community based study (AMSTEL).
      ]. It has also been associated with re-hospitalization [
      • Mistry R.
      • et al.
      Social isolation predicts re-hospitalization in a group of older American veterans enrolled in the UPBEAT program.
      ] and falls [
      • Faulkner K.A.
      • et al.
      Is social integration associated with the risk of falling in older community-dwelling women?.
      ].
      A cancer diagnosis and treatment are associated with high levels of stress, so much so that patients may develop cancer-related post-traumatic stress disorder [
      • Cordova M.J.
      • Riba M.B.
      • Spiegel D.
      Post-traumatic stress disorder and cancer.
      ]. Following a cancer diagnosis, individuals experience disruptions in their social networks and require greater amounts of social support, particularly older adults [
      • Kadambi S.
      • et al.
      Social support for older adults with cancer: young International Society of Geriatric Oncology review paper.
      ]. Patients with cancer who have higher levels of social support report improved quality-of-life [
      • Applebaum A.J.
      • et al.
      Optimism, social support, and mental health outcomes in patients with advanced cancer.
      ,
      • Lim J.W.
      • Zebrack B.
      Social networks and quality of life for long-term survivors of leukemia and lymphoma.
      ,
      • Sammarco A.
      • Konecny L.M.
      Quality of life, social support, and uncertainty among Latina breast cancer survivors.
      ,
      • Filazoglu G.
      • Griva K.
      Coping and social support and health related quality of life in women with breast cancer in Turkey.
      ,
      • Adam A.
      • Koranteng F.
      Availability, accessibility, and impact of social support on breast cancer treatment among breast cancer patients in Kumasi, Ghana: a qualitative study.
      ,
      • Li M.-Y.
      • et al.
      Effects of social support, hope and resilience on quality of life among Chinese bladder cancer patients: a cross-sectional study.
      ]. In breast cancer, lack of social support is an independent risk factor for toxicity from chemotherapy [
      • Magnuson A.
      • et al.
      Development and validation of a risk tool for predicting severe toxicity in Older Adults receiving chemotherapy for early-stage breast Cancer.
      ] and potentially cancer progression [
      • Nausheen B.
      • et al.
      Social support and cancer progression: a systematic review.
      ].
      In this current study, a population of older adults undergoing active treatment for cancer displayed low rates of loneliness and social isolation with higher levels of social support in the setting of the ongoing COVID-19 pandemic. However, females, those who live alone, and individuals with lower incomes were at higher risk of loneliness. Given the important implications of loneliness on both physical and mental health, our study indicates a separate screening for loneliness and social support may be necessary, particularly in these higher risk populations. Limiting screening to patients with significant comorbidities may fail to capture some patients.

      4.4 Future Directions

      Although the number of participants with severe loneliness in our study was low, almost one third of participants did report some form of loneliness, which may have important implications on mental and physical health. Even prior to the COVID-19 pandemic, the National Academies of Sciences, Engineering, and Medicine Consensus Study Report called on health care professionals to identify, prevent, and mitigate the adverse health impacts of social isolation and loneliness [
      • National Academies of Sciences, E. and Medicine
      Social isolation and loneliness in older adults: Opportunities for the health care system.
      ]. Numerous interventions have been evaluated to help reduce social isolation and loneliness [
      • Gardiner C.
      • Geldenhuys G.
      • Gott M.
      Interventions to reduce social isolation and loneliness among older people: an integrative review.
      ]. Interventions shown to be effective include group activities, animal interventions, befriending interventions, and leisure/skill development (Table 4). Unfortunately, many of these interventions involve in-person interactions that are not feasible during the COVID-19 pandemic [
      • Williams C.Y.K.
      • et al.
      Interventions to reduce social isolation and loneliness during COVID-19 physical distancing measures: a rapid systematic review.
      ]. Videoconferencing interventions have been previously shown to reduce levels of loneliness, although fewer studies have utilized this technology [
      • Tsai H.H.
      • et al.
      Videoconference program enhances social support, loneliness, and depressive status of elderly nursing home residents.
      ]. Beyond the COVID-19 pandemic, remote interventions may also be helpful for older adults who may have difficulties with mobility or transportation. Furthermore, remote interventions may be more scalable and economic.
      Table 4Existing Interventions to reduce social isolation.
      Types of interventionsDescriptionExampleEvidence
      Social facilitationFacilitating interactions with peersCircle of Friends [
      • Jansson A.
      • Pitkälä K.H.
      Circle of friends, an encouraging intervention for alleviating loneliness.
      ]
      Improvement of older adults' well-being, health, and cognition
      Psychological therapiesApproaches delivered by trained therapistsMindfulness and stress reduction [
      • Creswell J.D.
      • et al.
      Mindfulness-based stress reduction training reduces loneliness and pro-inflammatory gene expression in older adults: a small randomized controlled trial.
      ]
      Intervention reduced loneliness
      Health and social care provisionHealthcare professionals supporting older adultsCARELINK program [
      • Nicholson Jr., N.R.
      • Shellman J.
      Decreasing social isolation in older adults: effects of an empowerment intervention offered through the CARELINK program.
      ]
      Those receiving intervention were 12 times less likely to report social isolation compared to control group
      Animal interventionsFeline and canine companionsAnimal-assisted therapy [
      • Banks M.R.
      • Banks W.A.
      The effects of group and individual animal-assisted therapy on loneliness in residents of long-term care facilities.
      ]
      Effective in improving loneliness as individual animal-assisted therapy
      Befriending interventionsFormulating new friendshipsCall in Time [
      • Cattan M.
      • Kime N.
      • Bagnall A.M.
      The use of telephone befriending in low level support for socially isolated older people--an evaluation.
      ]
      Participants gained confidence and became socially active again
      Leisure developmentFocus on leisure or skill developmentInternet-at-home intervention [
      • Fokkema T.
      • Knipscheer K.
      Escape loneliness by going digital: a quantitative and qualitative evaluation of a Dutch experiment in using ECT to overcome loneliness among older adults.
      ]
      Improvements in emotional loneliness and self-confidence

      5. Conclusions

      Loneliness, social isolation and social support are overlapping domains which have important implications in the physical and mental health of older adults with cancer. The ongoing social distancing recommendations during the COVID-19 pandemic have potentially impacted these areas. In a cohort of older adults with cancer undergoing active treatment, there were relatively low rates of loneliness and social isolation and high rates of social support. Further studies are needed to investigate if a cancer diagnosis and treatment may mediate changes in loneliness, social isolation, and social support in the context of the pandemic and beyond.

      Declarations

      Funding Source: Cancer and Aging Research Group Pilot Grant.

      Author Contributions

      Conceptualization: Katherine Clifton, Tanya Wildes.
      Funding acquisition: Katherine Clifton.
      Project Administration: JoAnn Jabari, Mary Van Aman, Patricia Dulle.
      Data Curation: JoAnn Jabari, Mary Van Aman, Patricia Dulle.
      Formal Analysis: Katherine Clifton, Feng Gao, Janice Hanson, Tanya Wildes.
      Writing – original draft: All authors.
      Writing – review and editing: All authors.

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