Exploring the Impact of the COVID-19 Pandemic on Cancer-Related Distress Among Thoracic Oncology Patients at a Rural Cancer Center

doi:10.21203/rs.3.rs-3876631/v1

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Exploring the Impact of the COVID-19 Pandemic on Cancer-Related Distress Among Thoracic Oncology Patients at a Rural Cancer Center

https://doi.org/10.21203/rs.3.rs-3876631/v1

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Purpose: Cancer-related distress (CRD) is frequently observed in rural settings and may have been exacerbated during the COVID-19 pandemic. We examined pre and post COVID-19 changes in CRD among individuals treated for thoracic cancers at a rural cancer center.

Methods: Patient demographics, clinical information, and CRD measures derived from the National Comprehensive Cancer Network psychosocial distress problem list were abstracted from electronic medical records for thoracic oncology patients treated at a rural Michigan cancer center before (January 1, 2019-January 1, 2020; n=139) and during (January 20, 2020-January 31, 2021; n=84) the COVID-19 pandemic. CRD scores overall and by type (practical, emotional, social, and physical concerns) were calculated by summing the relevant problem list items. We assessed changes in CRD overall and by type using chi-square tests, Fisher’s exact tests, and multivariable logistic regression models.

Results: CRD prevalence increased by 9.1% during vs. before the pandemic (97.6% vs. 88.5%; p=0.02), with largest increases evident for emotional (82.1% vs. 64.0%; p=0.004) and physical (82.1% vs. 67.6%; p=0.02) concerns. CRD scores were slightly higher during vs. before the pandemic but the differences were not significant (all p-values>0.05). Compared to those treated in the year prior, patients treated during the pandemic had higher odds of elevated CRD (OR (95% CI) =1.86 (1.1, 3.2)), and practical concerns (OR (95% CI) =2.19 (1.3, 3.8)).

Conclusions: Findings from this preliminary study suggest an increased prevalence of CRD among rural thoracic oncology patients treated during compared to before the COVID-19 pandemic.

Cancer

psychosocial

distress

rural

oncology

COVID-19

Rural-urban cancer disparities in the U.S. are well documented, with higher overall cancer incidence and mortality rates in rural areas, where approximately 20% of the population resides [1, 2]. Individuals living in rural regions face multiple barriers to accessing oncology care, including limited transportation options, longer distances traveled to cancer treatment centers, lower access to clinical trials, workforce shortages, and lower health insurance coverage than their urban counterparts [3, 4]. Over 50% of rural U.S. counties have no oncologists, and 20% of rural residents must travel over 60 miles to access oncology services [5]. These healthcare access barriers contribute to higher healthcare costs and can amplify psychosocial and financial challenges for rural-dwelling individuals treated for cancer [6, 7, 8].

Cancer-related distress (CRD) is a complex and unpleasant experience encompassing psychological, social, spiritual and/or physical concerns, affecting between 25–60% of individuals with cancer [9, 10]. Rural residents report higher levels of CRD than their urban counterparts; in part due to lower socioeconomic resources (e.g., health insurance coverage) and limited access to healthcare services [11, 12, 13, 14]. The prevalence of CRD also varies according to cancer site, with individuals treated for thoracic cancer being particularly susceptible, possibly due to poor overall prognosis [9, 12, 13, 15, 16]. CRD has been associated with lower quality of life and poorer cancer-related outcomes such as treatment non-adherence, shorter time to disease progression, and increased mortality [17, 18, 19]. Given such clinical relevance, the National Comprehensive Cancer Network (NCCN) recommends routinely screening individuals for CRD throughout the cancer care continuum.

The COVID-19 pandemic and associated social distancing measures have been linked to dramatic increases in psychological distress and other mental health conditions such as anxiety, post-traumatic stress disorder, and depression [20, 21]. Growing evidence indicates that CRD has also increased since the onset of the pandemic [22, 23], and this may have more adversely affected individuals in rural areas with limited access to supportive services. Yet, the potential impact of the COVID-19 pandemic on CRD among rural cancer patients remains uncertain, with prior studies demonstrating varied results [24, 25].

Understanding the burden of CRD among rural cancer survivors can inform strategies to allocate appropriate resources and supportive care services in underserved rural oncology settings. Thus, the aim of this study was to examine changes in CRD among individuals treated for thoracic cancers at a rural cancer center before and after the onset of the pandemic. To better characterize factors that contribute to rural disparities in CRD, we also examined the specific factors that contribute to CRD in our rural study population.

We conducted a retrospective medical chart review study including all individuals treated through the Multidisciplinary Thoracic Oncology Program at Cowell Family Cancer Center, part of Munson Healthcare, before (January 1, 2019, through January 1, 2020; n = 139) and during (January 20, 2020, through January 31, 2021; n = 84) the COVID-19 pandemic. This time frame was chosen based on the date of the first diagnosed COVID-19 case within the United States. Munson Healthcare serves an entirely rural region in Northwest Michigan (county-level rural-urban continuum codes ranging from 5–9). Data on patient demographics (age at diagnosis, gender, and race), zip code of residence, cancer site (lung or esophageal), stage at diagnosis, and the NCCN psychosocial distress measures[26] were abstracted from the electronic medical records for all thoracic oncology patients treated during the study timeframes.

The NCCN guidelines include a specific problem-list questionnaire that assesses the prevalence of various factors contributing to CRD. Patients indicate their overall distress score on a Likert scale of 1–10, and then identify the presence or absence of specific symptoms from CRD areas, including practical, emotional, spiritual, social role and physical concerns.[27] This questionnaire has been validated using multiple mental health questionnaires.[28, 29] Practical concerns assessed in this study were derived from the NCCN problem list and included the following 11 items: needing help with daily living tasks, transportation, work or school, unable to afford household bills, unable to afford medical bills, worried about prescription coverage for oral medications, lack of medical coverage or high deductibles/copays, finding resources close to home, expressing choices about medical care, understanding treatment options, and other financial concerns. Emotional concerns encompassed the following 8 items: fears and worry about the future, depression, fear of medical procedures, losing control of things that matter, anger or feeling out of control, suicidal thoughts, feeling dependent on others, and changes in body image. Social role measures included questions related to concerns related to social role and family health issues. The following 13 physical concerns related to quality of life were also ascertained from the records: pain, sleep, fatigue, substance use, memory or concentration, sexual health, breathing, changes in urination, feeling swollen, fevers, skin dry or itchy, tingling in hands or feet, or other physical problems. For this study, we utilized data from the first completed CRD assessment, which was typically administered during the initial oncology visit following cancer diagnosis.

We described demographic and CRD characteristics of the study population overall and across timepoints (before vs. during the COVID-19 pandemic). Prevalence of CRD measures overall and by type were assessed and differences in these measures across time points were evaluated using chi-square and/or Fisher’s exact tests. The degree of CRD was calculated by summing the problem list items overall and by type (practical, emotional, social and physical concerns). The range of CRD summary scores were as follows: overall (0–22), practical (0–6), emotional (0–7), social (0–2), and physical (0–8).

We assessed changes in the mean and standard deviation of CRD summary scores before and during the pandemic using Student t tests. Using logistic regression models, we assessed both the odds of any vs. no CRD overall and by type and the odds of high vs. low CRD summary scores dichotomized at the median values (overall distress < = 5 vs. >5; practical < = 1 vs. >1; emotional < = 1 vs. >1; physical < = 2 vs. >2). Dichotomizing the CRD summary score for social concerns at the median resulted in the same categorization as the prevalence of social concerns. Thus, we did not consider the degree of social concerns in the model. We estimated odds ratios (OR) and 95% confidence intervals (CI) for associations of CRD measures in relation to the pandemic timepoints. We used backward selection of covariates in a multivariable logistic regression models, considering age (continuous), distance to cancer center in miles (calculated from residential zip code and categorized as < 10, 10-<25, 25-<50, 50+), gender (female, male), race (White, American Indian/Alaska Native, Other), cancer site (lung/esophagus), cancer stage at diagnosis (I, II, III, IV, missing). In secondary analyses, we assessed differences in the prevalence of CRD overall and by type according to participant characteristics using chi-square tests. Abstracted de-identified data were stored in a password-protected spreadsheet for analysis using SAS v9.4 (Cary, NC). The study was approved by the Institutional Review Boards at Michigan State University and Munson Medical Center.

A total of 223 individuals treated for thoracic cancers were included in the study (n = 139 before and n = 84 during the pandemic). As shown in Table 1, the mean age of the study population was 69.5 years, and most participants were male (61.0%) and White (95.5%). Over 20% of participants traveled 50 or more miles to the cancer center. Lung cancer was the most common cancer diagnosis (85.2%) and 30% of cancers were diagnosed at Stage I. Participant characteristics were generally similar across the study time points. However, a larger percentage of participants traveled 50 or more miles to the cancer center and were missing information on stage at diagnosis during vs. before the pandemic (26.2% vs. 19.4% and 47.6% vs. 15.1%, respectively).

Table 1

Characteristics of individuals treated for thoracic cancer before and during the COVID-19 pandemic.
	Overall (n = 223)	Before the COVID-19 Pandemic (n = 139)	During the COVID-19 Pandemic (n = 84)
Age, years	69.5 (9.7)	69.7 (10.3)	69.1 (8.5)
Distance to cancer center, miles
<10	58 (26.0)	39 (28.1)	19 (22.6)
10 to < 25	44 (19.7)	25 (18.0)	19 (22.6)
25 to < 50	72 (32.3)	48 (34.5)	24 (28.6)
50+	49 (22.0)	27 (19.4)	22 (26.2)
Gender
Female	87 (39.0)	48 (34.5)	39 (46.4)
Male	136 (61.0)	91 (65.5)	45 (53.6)
Race
White	213 (95.5)	134 (96.4)	79 (94.1)
American Indian/Alaska Native	5 (2.2)	4 (2.9)	1 (1.2)
Other	5 (2.2)	1 (0.7)	4 (4.8)
Cancer Site
Esophagus	33 (14.8)	19 (13.7)	14 (16.7)
Lung	190 (85.2)	120 (86.3)	70 (83.3)
Stage at diagnosis
I	67 (30.0)	54 (38.9)	13 (15.5)
II	24 (10.8)	15 (10.8)	9 (10.7)
III	50 (22.4)	33 (23.7)	17 (20.2)
IV	21 (9.4)	16 (11.5)	5 (6.0)
missing	61 (27.4)	21 (15.1)	40 (47.6)
Values are mean (sd) or N (%)

Over the entire study period, 91.1% of participants reported CRD, 84% reported practical concerns, 70.9% reported emotional concerns, 22.0% reported social concerns and 73.1% reported physical concerns. As shown in Fig. 1, the prevalence of any CRD increased by 9.1% during vs. before the pandemic (97.6% vs. 88.5%; p = 0.02). The largest increases during vs. before the pandemic were observed for emotional (82.1% vs. 64.0%; p = 0.004), and physical (82.1% vs. 67.6%; p = 0.02) concerns, while non-significant increases were also evident for practical (89.3% vs. 79.1%; p = 0.05) and social concerns (23.8% vs. 20.9%; p = 0.61).

As shown in Table 2, mean CRD scores were slightly higher during vs. before the pandemic but the increase was not significant (6.3 vs. 5.4; p = 0.08). Mean CRD scores for practical, emotional, and physical concerns were also non-significantly higher during vs. before the pandemic (all p-values ≥ 0.05). Conversely, CRD scores related to social concerns did not change across study points (0.26 vs. 0.26; p = 0.97). Many of the specific problems contributing to CRD, particularly those related to social and physical concerns, remained relatively unchanged across groups. However, we observed a higher prevalence of needing help with daily tasks (25.0% vs. 8.6%; p = 0.001) and other financial concerns (13.1% vs. 2.2%; p = 0.003), and a lower prevalence of problems related to work or school (0.0% vs. 7.2%; p = 0.01) and concerns related to expressing choices about medical care (4.8% vs. 18.0%; p = 0.004) during vs. before the pandemic. Fears and worry about the future were more commonly reported during vs. before the pandemic (60.7% vs. 40.3%; p = 0.003). Interestingly, a lower percentage of individuals reported losing control of things that mattered during vs. before the pandemic onset (3.6% vs. 12.2%; p = 0.03). Finally, a significant increase in the percentage of participants reporting changes in urination was observed during vs. before the pandemic (14.3% vs. 5.0%; p = 0.02). While not significant, participants were more likely to report distress related to feeling dependent on others (45.2% vs. 33.1%; p = 0.07) and fear of medical procedures (16.7% vs. 9.4%; p = 0.10) during vs. before the pandemic. While we did not observe any changes across the study time points, we observed the highest prevalence of concerns related to understanding treatment options (70.4%), fear and worry about the future (48.0%), fatigue (46.2%), sleep concerns (40.8%), feeling dependent on others (37.7%), depression (36.8%), pain (35.4%), and breathing issues (32.3%).

Table 2

Psychosocial distress summary scores and specific concerns before and during the COVID-19 pandemic.
	Overall (n = 223)	Before the COVID-19 Pandemic (n = 139)	During COVID-19 Pandemic Rural (n = 84)	p-value
Distress Summary Scores, mean (sd)
Overall Distress (range 0–22)	5.7 (4.0)	5.4 (4.1)	6.3 (3.7)	0.08
Practical Concerns (range 0–6)	1.5 (1.1)	1.4 (1.1)	1.7 (1.0)	0.06
Emotional Concerns (range 0–7)	1.5 (1.4)	1.4 (1.4)	1.8 (1.4)	0.05
Social Concerns (range 0–2)	0.26 (0.5)	0.26 (0.5)	0.26 (0.5)	0.97
Physical Concerns (range 0–8)	2.2 (1.9)	2.0 (1.9)	2.4 (1.9)	0.13
Practical Concerns, %
Need help with daily living tasks	14.8	8.6	25.0	0.001
Transportation	17.0	17.3	16.7	0.91
Work or school	4.5	7.2	0.0	0.01
Unable to afford household bills	2.7	2.9	2.4	0.99
Unable to afford medical bills	13.9	14.4	13.1	0.79
Worried about prescription coverage for oral medications	11.2	9.4	14.3	0.26
Lack of medical coverage or high deductibles/copays	11.7	10.8	13.1	0.60
Finding resources close to home	7.6	8.6	6.0	0.46
Expressing choices about medical care	13.0	18.0	4.8	0.004
Understanding treatment options	70.4	68.4	73.8	0.39
Other financial concerns	6.3	2.2	13.1	0.003
Emotional Concerns, %
Fears and worry about the future	48.0	40.3	60.7	0.003
Depression	36.8	36.7	36.9	0.97
Fear of medical procedures	12.1	9.4	16.7	0.10
Losing control of things that matter	9.0	12.2	3.6	0.03
Anger or feeling out of control	2.2	1.4	3.6	0.37
Suicidal thoughts	0.5	0.7	0.0	0.99
Feeling dependent on others	37.7	33.1	45.2	0.07
Changes in body image	5.4	3.6	8.3	0.13
Social Concerns, %
Concern with social role	8.1	8.6	7.1	0.69
Family health issues	17.9	17.3	19.1	0.74
Physical Concerns, %
Pain	35.4	35.3	35.7	0.94
Sleep	40.8	37.4	46.4	0.18
Fatigue	46.2	43.2	51.2	0.24
Substance use	7.6	5.8	10.7	0.18
Memory or concentration	12.1	12.2	11.9	0.94
Sexual health	1.4	0.7	2.4	0.56
Breathing	32.3	29.5	36.9	0.25
Changes in urination	8.5	5.0	14.3	0.02
Feeling swollen	4.5	2.9	7.1	0.18
Fevers	0.9	1.4	0.0	0.53
Skin dry or itchy	9.4	9.4	9.5	0.97
Tingling in hands or feet	15.3	15.8	14.3	0.76
Other physical problems	3.1	3.6	2.4	0.71
Numbers represent mean (standard deviations)

Patients treated during vs. before the pandemic had 5.33 higher odds (95% CI = 1.20, 23.8) of experiencing CRD, 2.20 higher odds of experiencing emotional concerns (95%CI = 1.3, 5.0) and 2.16 higher odds of reporting physical concerns (95% CI = 1.1, 4.2). In models of CRD severity, higher levels of distress overall (OR (95% CI) = 1.86 (1.1, 3.2)), and for practical concerns, specifically (OR (95% CI) = 2.19 (1.3, 3.8)) were observed during the pandemic, as shown in Table 3. Of note, none of the factors were retained in the multivariable models except for the model of any physical concerns, where age was included.

Table 3

Odds ratios and 95% confidence intervals for psychosocial distress overall and by type during vs. before the COVID-19 pandemic.
	Odds Ratio (95% CI) Any vs. None	Odds Ratio (95% CI) High vs. Low
Overall Distress	5.33 (1.2, 23.8)	1.86 (1.1, 3.2)
Practical Concerns	2.20 (0.98, 4.9)	2.19 (1.3, 3.8)
Emotional Concerns	2.58 (1.3, 5.0)	1.24 (0.7, 2.1)
Social Concerns	1.19 (0.6, 2.3)	n/a
Physical Concerns	2.16 (1.1, 4.2) *	1.38 (0.8, 2.4)
*Models used backward selection of covariates including age, cancer site, race, stage at diagnosis, and distance traveled to hospital. Age was retained in the model for Physical Concerns (Any vs. None) only. No covariates were retained in other models.

In secondary analyses shown in Supplemental Table 1, the prevalence of psychosocial distress overall and by type did not differ by distance traveled to cancer center (all p ≥ 0.45), gender (all p ≥ 0.34), race (all p ≥ 0.11), cancer site (all p ≥ 0.42), or cancer stage at diagnosis (all p ≥ 0.46). However, physical concerns were more commonly reported among those aged 50 to 74 years compared to both the younger and older age groups.

Findings from this study suggest a high overall burden of CRD among individuals treated for thoracic cancers at a rural oncology clinic, with increasing prevalence after the onset of the COVID-19 pandemic. Distress in this population was most commonly related to practical, emotional and physical concerns, including difficulty understanding treatment options, fear and worry about the future, fatigue, and sleep concerns. Notably, patients treated during the pandemic were more likely to experience CRD related to emotional and physical concerns compared to those treated in the year before the pandemic. CRD related to social concerns was less commonly reported, and the prevalence of social concerns did not change during the pandemic. Finally, a higher severity of CRD, and severity of distress related to practical concerns specifically, was reported during compared to before the pandemic.

The high prevalence of CRD among rural cancer survivors in this study is consistent with results from prior studies, which have observed a higher burden of psychosocial distress among rural cancer survivors compared to their urban counterparts [22, 23]. Consistent with these findings, the prevalence of psychosocial distress in our study was higher than that reported in other oncology settings [30, 31, 32]. Importantly, our findings also suggest that COVID-19 may have had a significant impact on psychosocial distress of rural-dwelling patients with cancer. These findings are consistent with results from a rapid review of 15 articles, which observed disproportionate psychosocial consequences of COVID-19 among individuals treated for cancer in rural regions [23]. Our results also align with previous studies demonstrating the adverse impact of the COVID-19 pandemic on health-related quality of life among rural cancer survivors [25, 33]. Conversely, a study comparing urban and rural cancer populations in Utah did not observe any significant differences in psychosocial distress indicators of social interactions, loneliness, financial strain, or accumulating difficulties after the onset of COVID-19 [24]. Moreover, no significant changes in psychosocial distress were observed after the onset of COVID-19 among individuals treated for breast cancer at an urban hospital in Germany [25, 34]. Discrepancies in findings across studies may be due to differences in access barriers across geographical locations [25], and/or differences in cancer site, and social determinants of health, which could differentially impact experienced distress and quality of life measures [9, 11, 29, 35].

Our findings build on results from prior studies by providing nuanced insight into the specific factors contributing to the higher burden of CRD among individuals treated for thoracic cancer in rural settings. The most commonly reported CRD concerns in our study population included depression, problems with breathing, fatigue and sleep problems, feeling dependent on others, and fears and worries about the future. These findings are generally consistent with results from a prior multicenter study conducted in Germany [31], although practical issues like transportation difficulties were notably higher in our rural study population. Importantly, over 70% of patients in this study reported problems understanding treatment options. This high burden may reflect the complexity of treatment associated with thoracic oncology [36], low health literacy [37], and the lack of supportive and educational resources for patient education in rural oncology settings [37]. Taken together, our findings regarding the prevalence of these key concerns contributing to CRD should be prioritized as areas of need for supportive care services in under-resourced rural oncology settings.

In our study, most specific problems related to CRD did not change during the pandemic period. However, several significant differences across time points were observed. The higher proportion of patients reporting needing help with daily tasks, other financial concerns, and fears and worries about the future during the pandemic are somewhat unsurprising given the well-described challenges associated with social distancing and fears surrounding the novel COVID-19 virus. Our findings that fewer participants reported feelings of losing control of things that mattered, problems related to work or school and concerns related to expressing choices about medical care during than before the pandemic onset, may be partially attributable to implications of the pandemic on daily life, including flexible work arrangements[38], and on collective values and perspectives in a time of tremendous uncertainty [39]. Interestingly, we observed an unexpected higher proportion of patients reporting changes in urination during vs. before the pandemic; although the proportion of patients reporting these symptoms was somewhat minimal (i.e., < 15%). COVID-19 has been linked to urinary incontinence in several small studies [29, 40]; though we did not have information on COVID-19 infection status in this study population. Comparable to findings from another study of rural cancer survivors [41], we did not observe changes in depression after the onset of the pandemic. However, it is important to recognize that the prevalence of depression in our study population (~ 37%) was higher than the average in the general population, which ranges from 8–24%.³² Moreover, findings from several other studies have suggested increases in mental health problems in response to the pandemic [30, 35]. The discrepancy in findings across studies is likely multifactorial, and may be influenced by differences in perceptions of infection risk and control, cancer treatment discontinuation and quarantine regimens [18, 42, 43]. Additional research is needed to more comprehensively understand the potential short- and long-term consequences of the pandemic on cancer-related psychosocial distress measures.

The prevalence of CRD in our study population did not differ based on participant characteristics, except for age differences in physical concerns. For example, most participants reported physical concerns across all age groups, but the prevalence was higher in those between 50 and 74 years of age. Some of the physical concerns assessed in this study are associated with older age (e.g., memory or concentration)[44], although it is unclear why physical concerns would be less common in both the youngest and oldest age groups. Given the exploratory nature of this study, and the relatively small sample size, further research is needed to confirm this finding. We did not observe any significant gender differences in the prevalence of CRD, which differs from the findings of Mehnert et al., where women were more likely to report nearly every physical and CRD indicator on the NCCN problem list [31]. Discrepancy in findings may be due to our focus only on thoracic oncology patients, or because we categorized problems by type in our analysis, instead of considering gender differences across each individual problem measure. Although the average distance traveled to the cancer center for this rural population exceeded that of urban dwellers (8 miles) [41], and may contribute to increased burden, we did not observe any differences in psychosocial distress prevalence with increased distance traveled to receive oncology care in this study.

Strengths of this study include the focus on rural cancer survivors, an under-resourced population facing persistent disparities in cancer outcomes, and substantial healthcare access barriers that were heightened during the COVID-19 pandemic [45,46]. Furthermore, the survey used in this study was based on the widely recognized and validated NCCN distress problem list, which facilitates comparative findings across other studies of cancer survivors [47,48]. There were, however, several limitations to this study. The timing of the NCCN distress survey assessment varied across study participants and across the cancer care continuum. This variation may have influenced the degree of distress reported by individuals, with prior studies suggesting heightened distress within the first month post-diagnosis [48]. We also did not have information on socioeconomic indicators, cancer treatment or COVID-19 infection status in this study, which could have significantly influenced CRD measures. Finally, given that this study was conducted at a single rural oncology center and included a relatively small sample size of individuals treated for thoracic cancers, findings may not be generalizable in other settings or populations.

In summary, findings from this study demonstrate a significant and increasing burden of CRD among rural Michigan thoracic oncology patients treated during the COVID-19 pandemic. These findings underscore the potential impact of the pandemic on cancer-related distress and can inform targeted strategies to allocate limited resources to reduce the burden of CRD in underserved populations. Potential strategies to address the complex psychosocial challenges facing individuals treated for cancer in rural settings include using telemedicine approaches to address transportation barriers [49], fostering community-academic partnerships to extend the reach of evidence-based psychosocial interventions [50], and expanding access to supportive care services and palliative care in rural oncology settings [51]. Additional etiologic research is necessary to identify root causes of geographic differences in cancer-related psychosocial distress during the COVID-19 pandemic.

Ethical Approval and Accordance Statement

The Institutional Review Boards at Munson Healthcare and Michigan State University approved this retrospective chart review study (IRB IDs 1709562 & 1577790). The study was performed in accordance with the ethical standards as laid down in the 1964 Declaration of Helsinki.

Funding

No funding was received for conducting this study.

Author Contribution

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Sierra Silverwood, Douglas Peters, and Kelly Hirko. The first draft of the manuscript was written by Sierra Silverwood and Douglas Peters. Kelly Hirko, Yelena Kier, and Veronica Bernacchi supported and provided feedback during the writing process. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Acknowledgements

We would like to thank Cindy Michelin at the Cowell Family Cancer Center for providing guidance with electronic medical record review.

Data Availability Statement

The de-identified datasets analyzed for this study may be obtained by contacting the corresponding author.

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Exploring the Impact of the COVID-19 Pandemic on Cancer-Related Distress Among Thoracic Oncology Patients at a Rural Cancer Center

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