Cancer Treatment During COVID-19: Resilience of Individuals With Advanced Non–Small Cell Lung Cancer Versus Community Controls

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  • 1 Department of Psychology,
  • | 2 Comprehensive Cancer Center,  and
  • | 3 Division of Medical Oncology, Department of Internal Medicine, College of Medicine, The Ohio State University, Columbus, Ohio.

Background: Among all patients with cancer, those with advanced non–small cell lung cancer (NSCLC) experience the most distress. Although new therapies are improving survival, it is unknown whether receiving immunotherapy or targeted therapy during the COVID-19 pandemic increases patients’ psychological vulnerability. To meet clinical needs, knowledge of patients’ COVID-19 perceptions and safety behaviors is essential. Thus, this study compared patients’ psychological responses at diagnosis and during COVID-19 and compared patients with similar individuals without cancer during the same period. Patients and Methods: Patients with advanced NSCLC enrolled at diagnosis for cohort study participated (ClinicalTrials.gov identifier: NCT03199651). Those with follow-ups from April 28, 2020, through July 14, 2020 (n=76), were assessed again including COVID-19 measures. Simultaneously, community controls with similar sociodemographics and smoking histories were solicited (n=67). Measures were COVID-19 perceptions (Brief Illness Perception Questionnaire), social distancing, and depressive (Patient Health Questionnaire-9) and anxiety (Generalized Anxiety Disorder-7) symptoms. First, analyses evaluated differences in the psychological responses of patients with NSCLC at diagnosis and during COVID-19. Second, patients and controls were contrasted on COVID-19 perceptions, social distancing, and psychological symptoms. Results: The depressive and anxious symptoms of patients with NSCLC were greater at diagnosis (P<.02) than during COVID-19, approximately 1 year later. Patients with NSCLC and controls did not differ in terms of sociodemographics, except those with NSCLC were more racially diverse and older, and had greater smoking history (P<.03). Groups did not differ regarding concern, understanding, or perceived control over COVID-19 (P>.406). Notably, controls anticipated the COVID threat would last longer, practiced more social distancing, were more concerned about family (P<.04), and reported worse psychological symptoms (P<.023). With less depression and anxiety, patients with NSCLC viewed COVID-19 as a shorter-term threat and had fewer COVID-19–related worries than did controls. For controls, COVID-19 was more salient, heightening worries and psychological symptoms. Conclusions: Despite multiple health stressors, patients with NSCLC demonstrated resilience when receiving cancer treatment during COVID-19. Nonetheless, this population remains psychologically vulnerable, requiring support at diagnosis and thereafter.

Background

Patients with cancer are more vulnerable to COVID-19 than otherwise healthy individuals. Patients with lung cancer (LC) are uniquely vulnerable to coronaviral pneumonias (severe acute respiratory syndrome coronavirus 2 [SARS-CoV-2]), along with acute respiratory distress syndrome, and if infected, have a greater likelihood of dying.1,2 COVID-19 notwithstanding, the scope of the LC problem is without parallel.3 In the United States, LC accounts for 25% more cancer deaths than deaths from prostate, breast, and colon cancers combined,4 partly because 84% of patients with LC are diagnosed at an advanced stage.5 Non–small cell LC (NSCLC) accounts for 85% of all LCs and is the fifth costliest tumor to treat, with estimated national expenditures of $14.7 billion for 2020.6

As the pandemic continues, patients with LC are, unfortunately, vulnerable for other reasons: they are the most emotionally distressed of all cancer groups,7 having the greatest prevalence of mood and anxiety disorders.8 At diagnosis, many patients with advanced (stage IV) NSCLC perceive cancer as consequential and uncontrollable, even in the context of new immunotherapy and targeted treatments.9 Approximately 40% report moderate to severe depressive symptoms, anxiety, and trauma levels of cancer-specific stress,10 and cross-sectional studies postdiagnosis show heightened symptom levels.11,12 Many might assume that COVID-19 adds further stress to patients with NSCLC, although the extent to which this occurs is unknown. It is possible, however, that this population actually exhibits a positive adaptation known as resilience, which is the ability to maintain or regain mental health despite experiencing adversity.13 Without information, providers may be ill-prepared to meet patients’ needs during this difficult time and may not know the extent to which COVID-19 exacerbates patients’ stress, particularly as they try to continue therapy during the pandemic. Such issues are time-sensitive, considering the devastation attributable to mental health consequences of the pandemic,14 the multiple waves of COVID-19 cases in the United States, and the stalling of vaccine uptake.15

Patients with NSCLC, enrolled at diagnosis and followed for a cohort study (ClinicalTrials.gov identifier: NCT03199651), enabled analysis of 2 important issues. First, patients’ psychological responses at diagnosis (pre–COVID-19) were compared with those during COVID-19. Prior to COVID-19, many cancer groups have shown a declining trajectory of stress or depression from diagnosis across time.1618 We were uncertain if that trend would still be evidenced with patients in treatment amid the pandemic. Second, the responses of patients with NSCLC during COVID-19 were compared with a time-equivalent normative sample, namely, similar individuals from the community also coping with COVID-19 but cancer-free. Having health risk from multiple sources, would patients with NSCLC show greater negative affect, such as pessimism or worry, or difficulties with social distancing than others trying to cope while free of the added cancer burden? Relevant to clinical care, would the picture for patients with LC be one of unique, added burden or one, possibly, of resilience?

The study was performed in Ohio as infections were beginning to increase in April 2020. At that time, 750 new cases were occurring per day (21,000 total), a rate that remained stable until early June 2020. Thereafter, cases accelerated at more than double the daily rate (n=1,630) and approached a total nearly 4 times higher (n=78,000) by the end of data collection (July 2020). Patients with NSCLC still enrolled and alive completed a COVID-19–specific assessment during the study window; archival psychological data from the patients at diagnosis were also used. As COVID-19 risk varies across time and US states, data from comparison individuals (controls) residing in Ohio were obtained during the same window.

Patients and Methods

Procedures

The Institutional Review Board of The Ohio State University approved the study and all procedures in accordance with the Declaration of Helsinki. All participants completed written informed consent. A group comparison design was used.

The NCI-designated Ohio State University Comprehensive Cancer Center enrolled patients with stage IV NSCLC at diagnosis into an observational cohort (Beating Lung Cancer in Ohio [BLCIO]; ClinicalTrials.gov identifier: NCT03199651) beginning in 2017. Supplemental eTable 1 provides inclusion/exclusion criteria (available with this article at JNCCN.org). Patient-reported outcomes for anxiety and depressive symptoms were completed by telephone at diagnosis with the aid of a survey research firm. In the same manner, patient follow-ups scheduled from April 28, 2020, to July 14, 2020, were performed with COVID-19–specific items additionally completed. Of the 99 patients to be assessed in the time window, 76 were completed (76.8%). Reasons for the 23 missing responses were: 4 too ill to complete assessment; 9 contacted but not completed before assessment window (30 days) closed; and 10 not contacted within assessment window. Overall, BLCIO has a mean completion rate of 80% of available patients (those still alive) across follow-ups from diagnosis to 24 months.

Published data from the cohort at diagnosis (n=186 through April 2019) showed a mean age of 62.5 years, 91.4% with a smoking history, low education and income levels, and all patients residing in Ohio.10 These characteristics guided the solicitation of controls. Because difficulty with matching was anticipated, 2 web-based platforms (ResearchMatch, CloudResearch) were used with the following participation criteria: no prior or current cancer diagnosis, age 45–90 years, high school education or less, ≤$75,000 annual income, current or former smoker, Ohio resident, and ability to complete online assessments in English. From May 8, 2020, to June 19, 2020, 67 control individuals enrolled and completed measures on Qualtrics.

Measures

Psychological Symptoms

ASCO-recommended measures were used.19 Symptoms of major depressive disorder were assessed using the Patient Health Questionnaire-9 (PHQ-9)20 measure. The PHQ-9 total score can range from 0 to 27, with each of 9 items measured on a Likert scale from 0 (not at all) to 3 (nearly every day). Symptoms of generalized anxiety disorder were assessed with the Generalized Anxiety Disorder-7 (GAD-7)21 measure. The GAD-7 total score can range from 0 to 21, with each of 7 items measured on the same Likert scale as the PHQ-9. Cutoffs suggestive of at least moderate symptom levels are >9 for both measures.

General Health Concern

Patients with NSCLC rated the following item: “Has the COVID-19 pandemic worsened your concern about your lung cancer?,” and controls rated “Has the COVID-19 pandemic worsened your concern about your health?” The scale for each ranged from 0 (not at all concerned) to 10 (extremely concerned).

COVID-19 Measures

Illness Perceptions

The Brief Illness Perception Questionnaire22 assessed patients’ and controls’ perceptions of COVID-19 (its consequences, timeline, personal control, concern, understanding). For example, the timeline item asked, “How long do you think the COVID-19 pandemic will continue?” The concern item asked, “How concerned are you about getting COVID-19?” Each item was rated from 0 to 10. Two items that were not relevant to COVID-19 were omitted (treatment control, identity/symptoms) (see supplemental eTable 2 for complete description).

Exposure, Social Distancing, and Stress/Worry

For infection tally, items from Wang et al23 were used. Three items assessed knowledge (number) of persons with COVID-19 in the family, friends, and acquaintances (eg, “How many family members have been diagnosed with COVID-19?”). For social distancing, one item was used, which was rated from 0 (not at all) to 6 (all the time): “Have you been able to ‘socially distance’ yourself from household members?” For stress and worry, 3 items were used. The questions “How would you rate your stress during isolation or social distancing?” and “Has isolation or social distancing created tension in your household?” were both rated on a 0- to 6-point scale, with higher scores indicating more stress/tension, and “How worried are you that any of your close family members will contract COVID-19?” was rated from 0 (not worried at all) to 10 (extremely worried) (see supplemental eTable 2 for complete description).

Descriptive

Sociodemographic items were included. For patients with NSCLC, data were obtained from the electronic medical record and verified by 2 raters. NSCLC disease and treatment characteristics were obtained as well as the Charlson comorbidity index (CCI)24 quantitatively summarizing the presence and severity of 17 common medical conditions. CCI scores ranged from 0 to 37; NSCLC scores were a minimum of 6 for “metastatic solid tumor.” Controls self-rated all CCI items.

Statistical Analysis

One-way ANOVAs and chi-square tests examined group differences in demographics. A Fisher exact test was run for race due to low variability (n=3 for non-White participants in the control group). Variables significantly different between groups were used as controls.

For the first analyses, paired sample t tests were used to test change in the depressive and anxiety symptoms from diagnosis (pre–COVID-19) to follow-up during COVID-19 of patients with NSCLC. Second, multivariate linear regressions tested for group differences in outcomes, controlling for variables significantly different by group. A P value <.05 was considered statistically significant. A sensitivity analysis using the g-power program25 was performed to confirm a sufficient sample size. Sensitivity analysis indicated a small–medium effect size of group differences in outcomes (f 2=0.106).

Results

Description

Patients With NSCLC

Comparing our sample to that of the SEER program,26 the NSCLC group was younger (mean, 62.6 years; range, 29–80 years), roughly equivalent in terms of sex (female, n=31; 40.8%), married/partnered (65.8%), and less ethnically/racially diverse (80.3% White) (Table 1). The sample was equivalent to SEER in that most of the tumors were adenocarcinoma (77.6%). Other sample characteristics included education level less than high school for 6.6% (n=5), high school for 35.5% (n=27), more than high school for 57.9% (n=44), and income, with 21.1% (n=16) below the Ohio poverty line for a family of 4 ($25,000). At follow-up, all patients except 5 were in treatment with novel immunotherapies or targeted therapies.

Table 1.

Cohort Characteristics

Table 1.

Controls: Comparison of Groups on Sociodemographics

Similarity of samples was approximated. NSCLC and control groups did not differ in terms of sex, education, income, marital status, or residence (Ohio). The control group was less diverse (5% vs 20% non-White; odds ratio [OR], 5.246; 95% CI, 1.447–19.024; P=.006), younger (59 vs 63 years; Cohen d=0.392; P=.023), and had somewhat fewer current/former smokers (75% vs 90%; OR, 2.890; 95% CI, 1.156–7.225; P=.020) (Table 1). Thus, the latter variables were entered as controls in the multivariate linear regression analyses.

Psychological Responses of Patients With NSCLC at Diagnosis Versus During COVID-19

Patients with NSCLC reported significantly more depressive (ΔM=1.737; 95% CI, 0.493–2.98; P=.007) and anxiety symptoms (ΔM=1.592; 95% CI, 0.264–2.920; P=.019) at diagnosis (pre–COVID-19) than during COVID-19. Percentages of patients with NSCLC above cutoff values at diagnosis and at COVID-19 follow-up were 17.1% (n=13) versus 11.8% (n=9) on the PHQ-9 and 15.8% (n=12) versus 13.2% (n=10) on the GAD-7, respectively.

Multivariate Linear Regressions Comparing Patients With NSCLC and Controls During COVID-19

Psychological Symptoms

Notably, patients with NSCLC reported significantly fewer depressive (β = −0.206; 95% CI, −4.142 to −0.355; P=.020) and anxiety symptoms (β = −0.196; 95% CI, −4.037 to −0.308; P=.023) than controls, with racial group, age, and smoking status controlled (Table 2). Percentages of individuals above cutoff values in the NSCLC and control groups were 11.8% versus 28.1% on the PHQ-9 and 13.2% versus 30.3% on the GAD-7, respectively.

Table 2.

Multivariate Regression Analyses of Depressive and Anxiety Symptoms, Perceptions, Exposure, Social Distancing, and Worries

Table 2.

Health Concern

COVID-19 worsened controls’ moderate concern about their health (mean score, 5.45), and interestingly, this was similar (P=.943) to the moderately worsening concern about cancer among patients with NSCLC (mean score, 5.91; Table 2).

COVID-19 Analyses

Illness Perceptions

Controlling for racial group, age, and smoking status, patients with NSCLC and controls perceived COVID-19 similarly. Both perceived they had high knowledge about COVID-19, felt they had similar (moderate) control over their own COVID-19 risk, and had similar levels of concern about contracting COVID-19. However, unlike patients with NSCLC, controls anticipated the COVID-19 threat would last significantly longer (β = −0.278; 95% CI, −0.925 to −0.180; P=.004).

Exposure, Social Distancing, and Stress/Worry

Controlling for relevant variables, groups did not differ on knowledge of persons with COVID-19. However, patients with NSCLC reported being significantly more successful with social distancing (β = 0.300; 95% CI, 0.217–0.979; P=.002), less stressed about COVID-19 (β = −0.177; 95% CI, −0.701 to −0.002; P=.049), and less worried about family contracting COVID-19 (β = −0.192; 95% CI, −0.734 to −0.028; P=.035) compared with controls.

Discussion

To our knowledge, this is the first empirical, controlled comparison study of the psychological and behavioral impacts of COVID-19 among US patients with cancer. The data are novel, because thus far, such studies have come from Europe and Asia only.27,28 Patients with LC are an important group, representing nearly 13% of all new cancer cases in the United States annually. Survival for those with advanced NSCLC is changing dramatically as new immunotherapies and targeted therapies become available and treatment guidelines shift regularly. Thus, it is important to understand and appreciate how patients with NSCLC with the most severe disease burden and symptom severity—ones uniquely susceptible to COVID-19 infection and death—are emotionally and behaviorally able to travel to the hospital and receive treatment, monthly if not weekly. Results are discussed in terms of the resilience of patients with NSCLC and the differential salience29 of COVID-19 for the controls. Implications for clinical practice are provided.

As noted,7 patients with LC are regularly identified with the highest levels of stress or depression, and depression at diagnosis predicts premature death for them (eg, hazard ratio, 1.39; 95% CI, 1.24–1.56).30 Pre-COVID-19, a downward trajectory of psychological symptom severity from diagnosis onward has been found for patients with cancer.1618 Some might view the significant declines in the psychological symptoms of patients with NSCLC from diagnosis to follow-up as a response shift.31 In response shift, patients recalibrate the meaning of questionnaire items, particularly if items are general, such as “rate your quality of life.” Response shift is unlikely for the PHQ-9/GAD-7 items, as they are the DSM-IV criteria for major depressive disorder and generalized anxiety disorder, and thus by design are not open to interpretation. The items have rigorous reliability and validity support. Therefore, we view the lower levels of depressive and anxiety symptoms of patients with NSCLC during COVID-19 as accurately reflecting their self-reported psychological status.

It is notable how low the patients’ PHQ-9/GAD-7 scores were during the COVID-19 pandemic. When designing the study, some expected the symptom scores to be elevated. To the contrary, the data characterize the patients as resilient in the face of COVID-19. Resiliency is adapting well in the face of adversity, trauma, tragedy, threats, or significant stress (colloquially, “being tough”).13,32 As defined, resiliency combines adversity or risk with positive outcomes, with the positive outcome often equated to a person “retaining their mental health and not succumbing to a mental illness.”33 Evidence for the resilience of patients with NSCLC includes reports of significantly less stress, less worry about their family contracting the virus, greater success with social distancing, and having no/few psychological symptoms at the time. This does not mean the patients with NSCLC were unfazed by the COVID-19 pandemic, because they had moderate concern about their lung cancer, but the latter was of similar magnitude to the controls’ concern about their health. These data contextualize the picture of how these patients with cancer are responding during the pandemic. That is, patients with NSCLC had cancer plus high COVID-19 risk and its associated comorbidities (eg, heart disease, chronic obstructive pulmonary disease), and the stigma of having a cancer that others view as self-imposed.34

Group differences may be also understood by differential salience of COVID-19. US studies have shown heightened COVID-19 anxiety and fear in the general population.35,36 For otherwise healthy controls without chronic conditions (CCI score = 2) and life routines unchanged, COVID-19 was a salient (ie, novel, unexpected) stressor. Compared with patients with NSCLC, controls reported significantly more stress, worry, and higher psychological symptoms, with more than twice the percentage of individuals scoring above diagnostic cutoffs for anxiety (13%) and depression (28%).37 Evidence for differential salience is, perhaps, most obvious in that controls were as concerned about their health as were individuals with advanced NSCLC. By contrast, COVID-19 for patients with NSCLC occurred in the midst of ongoing life threat, comorbidities, symptoms, and routines already disrupted by receiving cancer treatment.

Implications for clinical practice are considered (Table 3). Because data show that symptoms of depression and anxiety are higher at NSCLC diagnosis than thereafter, it is suggested that providers continually consider each patient’s timeline, especially during the COVID-19 pandemic. Providers may recognize resilience and also consider that patients with NSCLC continue to require supportive care to achieve survival benefits of new therapies. ASCO-recommended measures for depression and anxiety should be used at diagnosis and thereafter, and patients with positive screens would likely benefit from psychological treatment.

Table 3.

Implications for Clinical Practice

Table 3.

Research design and methodological aspects of the study are considered. This study addresses a gap, not only of psychological studies of patients with NSCLC receiving new therapies but also of patients with cancer during the COVID-19 pandemic. With any cross-sectional study of patients with cancer, it is relevant to appreciate the selection factor; in other words, the patients with NSCLC assessed during COVID-19 were those surviving “long enough” to reach an April 2020 follow-up, irrespective of time since diagnosis. However, the median time since diagnosis in this sample (∼1 year) highlights the improving prognosis being achieved with new therapies, a sharp contrast to the 4-month median observed for decades.38 Equivalence of geographic region and timing are key factors in choosing control conditions for studies of COVID-19. In general, it is difficult to obtain online research study volunteers for comparison with individuals who are older, have lower education/income, and have negative health behaviors such as smoking. We were fortunate that the strategy for control accrual resulted in no statistical differences in several social determinants of health, including marital/partner status, education, and income. Notably, the 2019 US Census poverty rate in Ohio was 13.1%, but 20% of individuals in both study groups live below the US-defined poverty line. Still, broad generalization of the control findings to similar others who are not research platform users is unknown.

Conclusions

New data provide perspective for appreciating the COVID-19 experience for patients with cancer at greatest risk. Patients with cancer may be more resilient to COVID-19 stressors than has been assumed or suggested.37 Although not immune to the stresses of COVID-19, data show resilience for otherwise heavily burdened patients with NSCLC—ones unable to “shelter in place” but leaving home regularly to receive treatment. Although recent data from >260,000 cancer survivors show patients with LC experience greater distress and disability and poorer quality of life than those with other common cancers,39 the latter studies do not necessarily capture the whole story. The present data show that, in the face of multiple health stressors and COVID-19, patients with NSCLC demonstrated resilience.

Acknowledgments

The authors wish to acknowledge the study participants for making this research possible and Dr. Samilia Obeng-Gyasi for comments on the manuscript. The authors acknowledge the Strategic Research Group, ResearchMatch, and CloudResearch for their contributions to data collection.

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Submitted February 22, 2021; final revision received June 7, 2021; accepted for publication June 18, 2021.

Author contributions: Study concept: Arrato, Andersen. Investigation: Arrato, Andersen. Data curation: Arrato, Coker, Covarrubias, Reisinger, Presley, Andersen. Formal analysis: Lo, Coker, Covarrubias. Funding acquisition: Shields. Methodology: Lo, Andersen. Supervision: Reisinger, Presley, Shields. Validation: Covarrubias. Writing – original draft: Arrato, Lo, Coker, Blevins, Andersen. Writing – review and editing: Arrato, Lo, Coker, Blevins, Reisinger, Presley, Shields, Andersen.

Disclosures: The authors have disclosed that they have not received any financial considerations from any person or organization to support the preparation, analysis, results, or discussion of this article.

Funding: This work was supported by funding from Ohio State University Comprehensive Cancer Center Pelotonia.

Correspondence: Barbara L. Andersen, PhD, Department of Psychology, The Ohio State University, 1835 Neil Avenue, Columbus, OH 43210-1222. Email: Andersen.1@osu.edu

Supplementary Materials

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