Background
The COVID-19 pandemic spread worldwide in January 2020 and led to national measures such as lockdowns and curfews in many parts of the world as soon as March/April 2020. This stressful event has deeply and lastingly impacted populations in health, psychological, social, and financial aspects.1,2 Posttraumatic stress disorder (PTSD) is defined as the direct or indirect exposure to a stressor (eg, actual or threatened death) followed by symptoms of intrusive memories, avoidance, and hyperarousal that persist for >1 month.3 PTSD and related disorders, such as anxiety, distress, and depression, have been reported during past pandemics, such as Ebola virus, severe acute respiratory syndrome, and H1N1 influenza, and their effects are compounded by the public health measures required, such as quarantine.4 The COVID-19 pandemic is unprecedented due to the repetition and duration of multiple waves of infections and lockdowns, and it may have deeper, long-term psychological consequences.
Some studies have reported high degrees of posttraumatic stress symptoms (PTSS) in the general population during the first wave of the COVID-19 pandemic, with a prevalence estimated at 27% in a meta-analysis.5 However, very few studies repeated these assessments to investigate changes in PTSS over time.6,7
Patients who have cancer may be particularly prone to developing PTSS due to a high baseline level of anxiety and depression in relation to their cancer diagnosis,8 the potential modification of cancer management in response to the COVID-19 pandemic,9 and a high risk of developing a severe form of COVID-19 infection.10–12 Several studies in various types of cancer reported PTSS in patients during the first wave of the pandemic, with a prevalence ranging from 9% to 35%.13–15 However, to our knowledge, there has been no longitudinal study to date following patients with cancer over the different waves of the pandemic.
As soon as April 2020, we set up a 1-year longitudinal prospective clinical cohort of patients with cancer (COVIPACT). Previously published baseline results showed that 21% of patients with cancer experienced PTSS associated with poor quality of life (QoL) during the first lockdown.16 An adjustment in medical oncology practice, such as cancellation or postponement of treatments or modification of follow-up, was implemented for approximately one-fourth of patients and was associated with the occurrence of PTSS. This article presents the longitudinal follow-up of the COVIPACT cohort. Our main objective was to describe the evolution of PTSS in patients with cancer over the first year of the COVID-19 pandemic and to identify factors associated with high PTSS. We also investigated the evolution of PTSS-related disorders (insomnia, cognitive complaints, and QoL)3,17 over the pandemic in relation to PTSS to better understand the global impact of PTSS induced by the COVID-19 pandemic.
Methods
Settings and Population
COVIPACT (NCT04366154) is a French longitudinal prospective study that enrolled patients between April 16 and May 29, 2020, and included outpatients aged ≥18 years and receiving oncologic treatment for solid or hematologic malignancy during the first nationwide lockdown at the day care hospital of 2 French cancer centers (the François Baclesse Center at Caen and the Henri Becquerel Center at Rouen).16 Patients receiving oral treatments and simple surveillance were not included.
Data Collection and Survey
Demographics, clinical information, history of oncologic disease, and pandemic-induced adjustment in medical oncology practices were collected from medical records. Inclusion was based on a nonopposition form distributed to patients at the oncologic day care hospital. At baseline, enrolled patients were asked to complete validated self-questionnaires assessing PTSS, insomnia, QoL, and cognitive complaints. Follow-up questionnaires were sent by mail every 3 months over the course of 1 year, which approximately matched the waves of the pandemic and related restrictions. Questionnaires were completed in April and May 2020 during the first French lockdown (M0), in July and August 2020 during the release period (M3), in October and November 2020 during the second French lockdown (M6), in January and February 2021 after the second lockdown release (M9), and in April and May 2021 during the third French lockdown (M12). Patients were included in the present study if they completed the questionnaire on PTSS at baseline and at least one follow-up.
Questionnaires
The Impact of Event Scale–Revised (IES-R) is a 22-item self-questionnaire that highlights avoidance, intrusion, and hyperarousal PTSS in relation to a prespecified stressful event.18,19 In COVIPACT, patients were asked to complete the IES-R questionnaire with regard to the COVID-19 pandemic. As previously recommended, a score of ≥33 out of 88 was used to identify moderate to severe PTSS.19
We used the Functional Assessment of Cancer Therapy–General (FACT-G) to assess QoL.20 It includes 27 items that measure the physical, social, emotional, and functional components of health-related QoL in patients with cancer and yields a total score of 108.
Insomnia was assessed using the 7-item Insomnia Severity Index,21 whose total score ranges from 0 to 28 and is interpreted as follows: absence of insomnia (0–7), subthreshold insomnia (8–14), moderate insomnia (15–21), and severe insomnia (22–28).
Cognitive complaints were evaluated by the Functional Assessment of Cancer Therapy–Cognitive Function (FACT-Cog),22 especially the Perceived Cognitive Impairment subscale that contains 20 items and yields a maximum score of 72. Clinically significant symptoms of cognitive complaints were defined as ratings lower than the 10th percentile of a normative sample.23
Patients completed a questionnaire about their living conditions and feelings during the first lockdown, including their family environment, education, occupational status, fears about COVID-19 infection, social interactions, feelings of social isolation, and self-reported use of psychotropic drugs.
Statistical Analysis
Data were described by number and proportion for categorical variables and mean and standard deviation for continuous variables. We used a logistic mixed model to describe the evolution of moderate to severe PTSS (IES-R score ≥33) over time. Models included an intercept representing baseline symptoms, a discrete time representing change of symptoms over time, and a random intercept for each patient to account for interindividual variability. To explore associations of factors with PTSS at baseline and their change over time, factors were entered as both simple effect and in interaction with time. First, factors were entered individually in models minimally adjusted for study center and progressive disease at 6 months. Then, factors were retained simultaneously in the final multivariable model if P<.10. In secondary analyses, we used mixed models to describe the evolution of QoL, cognitive complaints, and insomnia over time according to PTSS. We identified distinct trajectories of IES-R using latent class mixed models to identify patients with persistent or delayed PTSS over time. The optimal number of latent classes was chosen according to the Bayesian information criterion. The best statistical fit was reached with 4 trajectory groups, including 2 small trajectory groups of similar shape that were pooled a posteriori (supplemental eTable 1 and eFigure 1, available with this article at JNCCN.org). Multinomial logistic regression was then fitted to identify factors associated with each latent class trajectory.
All statistical analyses were carried out using R version 4.1.0 (R Foundation for Statistical Computing) using packages GLMMadaptive (version 0.8-0), lme4 (version 1.1-27.1), and lcmm (version 1.9.3). A 2-sided P value <.05 was considered statistically significant.
Ethical Approval
Approval for the study was obtained from the local ethics committee (ref. 220C07; South Mediterranean II Committee for the Protection of Persons). The study was conducted in compliance with the French research standard (MR-003 “Research in the Field of Health Without Collection of Consent”; compliance commitment to MR-003 for the François Baclesse Center [no.2146328v.0, dated from January 26, 2018]). All patients received information, and none expressed any opposition to the use of their data. COVIPACT is registered as IDRCB:2020- A00879-30 (ClinicalTrials.gov identifier: NCT04366154).
Results
Baseline Characteristics
We included 734 patients, including 565 who completed the IES-R. As previously published, no statistically significant differences were observed between sociodemographic and clinical characteristics, except for ECOG performance status ≥2, which was more frequent in 734 patients (P=.03).16 Among the 565 patients who completed the IES-R questionnaire at baseline, 386 completed at least 1 follow-up assessment and were included in the present longitudinal analysis (Figure 1). Mean follow-up was 9.7 months (range, 1.8–14.4 months). Most patients were female (76%), had breast cancer (50%), and had good general status (95% with ECOG performance status ≤1), and approximately half of the cohort had metastatic disease (Table 1). During the first lockdown, 15% of patients were living alone, 44% reported feeling socially isolated, and 66% worried about COVID-19 infection (Table 1). Clinical characteristics of the 386 patients retained in the longitudinal analysis and those of the initial 565 patients were similar (supplemental eTable 2). The IES-R score was also comparable between groups at baseline (mean [SD], 21.5 [15.5] and 20.8 [15.9], respectively).
Flowchart of patients with cancer in the French COVIPACT study.
Abbreviations: IES-R, Impact of Event Scale–Revised; M0, first French lockdown; M3, first French lockdown release; M6, second French lockdown; M9, second French lockdown release; M12, third French lockdown.
Citation: Journal of the National Comprehensive Cancer Network 21, 3; 10.6004/jnccn.2023.7085
Flowchart of patients with cancer in the French COVIPACT study.
Abbreviations: IES-R, Impact of Event Scale–Revised; M0, first French lockdown; M3, first French lockdown release; M6, second French lockdown; M9, second French lockdown release; M12, third French lockdown.
Citation: Journal of the National Comprehensive Cancer Network 21, 3; 10.6004/jnccn.2023.7085
Flowchart of patients with cancer in the French COVIPACT study.
Abbreviations: IES-R, Impact of Event Scale–Revised; M0, first French lockdown; M3, first French lockdown release; M6, second French lockdown; M9, second French lockdown release; M12, third French lockdown.
Citation: Journal of the National Comprehensive Cancer Network 21, 3; 10.6004/jnccn.2023.7085
Baseline Patient Characteristics (N=386)
Evolution of PTSS Over Time
During the first lockdown, 21.5% of patients had moderate to severe PTSS (Figure 2). The rate changed significantly over time (P<.001) with a marked decrease during the lockdown release (13.6% at M3), followed by a return to the same level as during the first lockdown during the second lockdown (23.2% at M6). The rate of patients with PTSS remained stable after the second lockdown (22.7% at M9) and slightly decreased at the end of follow-up (17.5% at M12). We observed a similar trend when using the IES-R scale as a continuous measure. All 3 PTSD components (avoidance, intrusion, and hyperarousal) followed a similar trajectory over time (data not shown).
Trajectory of PTSS in patients with cancer during the COVID-19 pandemic in the French COVIPACT study (n=386). Estimates and 95% confidence intervals are from a logistic mixed model on PTSS (defined as IES-R score ≥33) with discrete time and a random patient effect.
Abbreviations: IES-R, Impact of Event Scale–Revised; M0, first French lockdown (April–May 2020); M3, first French lockdown release (July–August 2020); M6, second French lockdown (October–November 2020); M9, second French lockdown release (January–February 2021); M12, third French lockdown (April–May 2021); PTSS, posttraumatic stress symptoms.
Citation: Journal of the National Comprehensive Cancer Network 21, 3; 10.6004/jnccn.2023.7085
Trajectory of PTSS in patients with cancer during the COVID-19 pandemic in the French COVIPACT study (n=386). Estimates and 95% confidence intervals are from a logistic mixed model on PTSS (defined as IES-R score ≥33) with discrete time and a random patient effect.
Abbreviations: IES-R, Impact of Event Scale–Revised; M0, first French lockdown (April–May 2020); M3, first French lockdown release (July–August 2020); M6, second French lockdown (October–November 2020); M9, second French lockdown release (January–February 2021); M12, third French lockdown (April–May 2021); PTSS, posttraumatic stress symptoms.
Citation: Journal of the National Comprehensive Cancer Network 21, 3; 10.6004/jnccn.2023.7085
Trajectory of PTSS in patients with cancer during the COVID-19 pandemic in the French COVIPACT study (n=386). Estimates and 95% confidence intervals are from a logistic mixed model on PTSS (defined as IES-R score ≥33) with discrete time and a random patient effect.
Abbreviations: IES-R, Impact of Event Scale–Revised; M0, first French lockdown (April–May 2020); M3, first French lockdown release (July–August 2020); M6, second French lockdown (October–November 2020); M9, second French lockdown release (January–February 2021); M12, third French lockdown (April–May 2021); PTSS, posttraumatic stress symptoms.
Citation: Journal of the National Comprehensive Cancer Network 21, 3; 10.6004/jnccn.2023.7085
Female patients, patients who felt socially isolated during the first lockdown, those who had fears of COVID-19 infection, and those who reported increased use of psychotropic drugs during this period had more PTSS at baseline. These associations remained broadly constant over time (supplemental eFigure 2), except for sex, whose effect tended to decrease over time (although not significantly; P for change =.32). In addition, patients who experienced any adjustment in medical oncology practices during the first lockdown tended to have more PTSS at baseline (P=.053), but the difference decreased over time (P for change =.002) toward no difference at M3 and thereafter. All these associations observed in minimally adjusted models remained similar when factors were considered simultaneously in a multivariable model (supplemental eTable 3).
We grouped patients into 3 homogeneous trajectory classes of IES-R change over time (Figure 3). Most patients were in the “stable low IES-R” class (n=295; 76.4%), characterized by a low IES-R score throughout follow-up. Other patients had a persistently moderate IES-R score over time, with either a subtle decrease during follow-up (“decreased moderate IES-R”: n=23; 6%) or a steep increase at second lockdown (“increased moderate IES-R”: n=68; 17.6%). As observed in the primary analysis, feelings of social isolation, fear of COVID-19 infection, and use of psychotropics were associated with the class trajectories (supplemental eTable 4).
Distinct trajectories of IES-R change over time in patients with cancer in the French COVIPACT study (n=386). Trajectory classes were identified by latent class linear mixed model on IES-R score. The optimal number of latent classes from 2 to 6 was chosen according to Bayesian information criterion. Four trajectory groups were identified, including one with a small sample size (n=5), which was combined a posteriori with another group with a similar trajectory, yielding 3 trajectory groups with distinct IES-R change over time. Each individual was assigned to the latent class with the highest probability of membership. The mean IES-R score estimate and 95% confidence interval over time are displayed for each latent class.
Abbreviations: IES-R, Impact of Event Scale–Revised; M0, first French lockdown (April–May 2020); M3, first French lockdown release (July–August 2020); M6, second French lockdown (October–November 2020); M9, second French lockdown release (January–February 2021); M12, third French lockdown (April–May 2021).
Citation: Journal of the National Comprehensive Cancer Network 21, 3; 10.6004/jnccn.2023.7085
Distinct trajectories of IES-R change over time in patients with cancer in the French COVIPACT study (n=386). Trajectory classes were identified by latent class linear mixed model on IES-R score. The optimal number of latent classes from 2 to 6 was chosen according to Bayesian information criterion. Four trajectory groups were identified, including one with a small sample size (n=5), which was combined a posteriori with another group with a similar trajectory, yielding 3 trajectory groups with distinct IES-R change over time. Each individual was assigned to the latent class with the highest probability of membership. The mean IES-R score estimate and 95% confidence interval over time are displayed for each latent class.
Abbreviations: IES-R, Impact of Event Scale–Revised; M0, first French lockdown (April–May 2020); M3, first French lockdown release (July–August 2020); M6, second French lockdown (October–November 2020); M9, second French lockdown release (January–February 2021); M12, third French lockdown (April–May 2021).
Citation: Journal of the National Comprehensive Cancer Network 21, 3; 10.6004/jnccn.2023.7085
Distinct trajectories of IES-R change over time in patients with cancer in the French COVIPACT study (n=386). Trajectory classes were identified by latent class linear mixed model on IES-R score. The optimal number of latent classes from 2 to 6 was chosen according to Bayesian information criterion. Four trajectory groups were identified, including one with a small sample size (n=5), which was combined a posteriori with another group with a similar trajectory, yielding 3 trajectory groups with distinct IES-R change over time. Each individual was assigned to the latent class with the highest probability of membership. The mean IES-R score estimate and 95% confidence interval over time are displayed for each latent class.
Abbreviations: IES-R, Impact of Event Scale–Revised; M0, first French lockdown (April–May 2020); M3, first French lockdown release (July–August 2020); M6, second French lockdown (October–November 2020); M9, second French lockdown release (January–February 2021); M12, third French lockdown (April–May 2021).
Citation: Journal of the National Comprehensive Cancer Network 21, 3; 10.6004/jnccn.2023.7085
PTSD-Related Symptoms
At all times, PTSS were strongly associated with insomnia, cognitive complaints, and poor global QoL (all P<.001; supplemental eFigure 3). In particular, at M6, when the differences between patients with and without PTSS were the greatest, 55% of patients with PTSS reported moderate to severe insomnia, and 40% had cognitive complaints, compared with 25% and 23% of patients without PTSS, respectively. In addition, there was an average difference of 8 points on the FACT-G global score of QoL throughout follow-up between patients with and without PTSS.
Discussion
This longitudinal prospective study of French patients with cancer followed over 1 year showed high levels of PTSS over the repeated waves of COVID-19 infections and associated lockdown periods, affecting almost one-fourth of patients who received medical oncology treatment. Female patients, patients who felt socially isolated during the first lockdown, those worrying about COVID-19 infection, and those who reported increased use of psychotropics during this period had more PTSS. PTSS were associated with more insomnia, more cognitive complaints, and worse QoL.
We observed 21.5% of moderate to severe PTSS at baseline at the beginning of the pandemic, which is similar to results of an Italian study of patients with lymphoma treated during the same period.13 A higher rate (35%) was observed in patients with breast cancer in Wuhan (China), which may be explained by the exclusively female population and the study location at the COVID-19 epicenter.14 Overall, the rate of PTSS in the cancer population appeared higher during this period than what is generally observed in nonpandemic contexts (6%–9%).17,24
Our results suggest that PTSS decreased in patients with cancer during the first lockdown release (summer 2020), affecting 13.6% of patients. This is in line with a French oncologic survey that identified 14.7% of patients with cancer with moderate to severe PTSS during the same release period.25 Our results are also consistent with data in the general population showing a decline in peritraumatic distress and anxiety from the early stages of lockdown to the release period.7,26 We also observed that the rate of PTSS increased again at the second lockdown, suggesting a link between the psychological distress of individuals and the series of restrictions and release periods. Although no longitudinal data are available on PTSS changes over time during the COVID-19 pandemic in patients with cancer, this further increase in symptoms was recently reported in a UK representative population survey.27 We hypothesize that COVID-19 leading to lockdowns was a factor of PTSS in addition to cancer, probably related to the distressing situation, life-threatening disease, modification of cancer treatments, and social isolation. However, we did not observe the same trend at the third lockdown, which could be explained by the advent of vaccination, less strict containment measures, and better understanding of COVID-19 infection, contributing to a potential resilience and decrease in fear of COVID-19, as observed in a German study.28
In our study, female sex, feeling socially isolated during the first lockdown, having fears of COVID-19 infection, and an increased self-reported use of psychotropic drugs were associated with PTSS. Female sex is a known risk factor for PTSD,3 which has also been reported in the context of the COVID-19 pandemic in cancer and general populations.7,13 Moreover, loneliness and worry about COVID-19 infection have been described as core features of the syndrome triggered by the pandemic.29,30 Besides, patients with PTSS had poor QoL and more cognitive and insomnia complaints, all of which are known to be associated with PTSD.3,17 In the context of the COVID-19 pandemic, sleep disturbances and impaired physical QoL have also been related to higher psychological distress.31,32
We identified 3 distinct trajectories of IES-R change over time. Although most patients had a stable low level of PTSS during the first year of the pandemic, almost one-fourth had moderate distress throughout the period, and, in particular, 17.6% showed worsened symptoms during the second lockdown. Mental health trajectories have already been investigated in the general population.26,33 A 6-week Chinese study conducted at the beginning of the pandemic found that half of the participants were resilient, 22% had delayed PTSD, 19% had recovered PTSD, and 15% had chronic PTSD.33 A UK longitudinal national survey found that approximately three-fourths of individuals had consistently good mental health during the first 6 months of the pandemic, whereas the others had consistent or worsened psychological distress at a far higher level than before the pandemic.26 Altogether, these results suggest that some psychological symptoms may be delayed in a substantial proportion of individuals, possibly because of the repetition of pandemic waves and associated social restrictions. We did not identify any specific factors associated with this delayed pattern of symptom onset, as compared with immediate PTSS onset, probably due to lack of power. However, considering a recent study assessing PTSD symptom trajectories, the delayed form may be associated with female sex and may be more frequent the later the age of the trauma exposure and the older the patients.34 This could explain the high proportion of delayed PTSS in our study, whereas this trajectory is expected to be a minority in the literature.35 Moreover, the delayed form could be associated with postevent stressors.36 In the case of the pandemic, it could be the reexposure related to the different waves. Reassuringly, these delayed forms seem to be associated with more resilience and fewer psychological consequences.34
The COVIPACT study is the first longitudinal study with a long follow-up of 1 year to assess PTSS and QoL in patients with cancer during the COVID-19 pandemic using validated questionnaires at different periods of lockdowns. However, this study has limitations. We used the IES-R self-questionnaire, which measures PTSS but does not allow a medical diagnosis of PTSD. Moreover, mental health conditions such as anxiety and depression, which are commonly intertwined with PTSD, were not assessed in our study and this may have made it difficult to interpret the PTSS.37,38 PTSD requires exposure to a specific traumatic event, and the question of whether the COVID-19 pandemic can be classified as a “sudden” and “catastrophic” trauma has been debated. For this reason, some authors have considered pandemic-induced PTSS as adjustment disorders.39 In the absence of a control group, we could not evaluate whether patients with cancer had prevalence or evolution of PTSS similar to the general population. However, our results were consistent with prevalence estimates from a meta-analysis in the general population5 and longitudinal trends over the repeated pandemic waves.7,26,27 Female patients represented a high proportion of our population, which may have led to overestimating PTSS. Finally, the high attrition rate and the loss to follow-up rate are the main limitations of our study. Attrition may be explained by the inclusion method based on the nonopposition form. The loss to follow-up rate may be explained by the repetition of questionnaires over time. More patients who did not experience disease progression completed the questionnaires, which is why we adjusted for this important factor in longitudinal analysis. Although the clinical characteristics and baseline IES-R score were comparable between patients who completed follow-up assessments and those who completed baseline assessments, we cannot exclude the possibility that attrition may have biased the assessment of PTSS over time.
Conclusions
Overall, we identified approximately one-fourth of patients with cancer with persistent PTSS over the first year of the COVID-19 pandemic. We hypothesize that lockdown periods could explain an increase in PTSS, and the approach to it must be particularly thoughtful in view of its potential psychological consequences, especially in PTSD at-risk populations such as patients with cancer. Long-term follow-up studies should shed light on the consequences of such psychological distress, especially in the field of oncology, where distress is correlated with poor adherence to treatment and survival.40 COVIPACT 2 (ClinicalTrials.gov identifier: NCT04747249), a study including the patients of COVIPACT with a moderate to severe level of PTSS, is underway to evaluate the benefit of psychological interventions to reduce them.
Acknowledgments
We acknowledge the Northwest Data Center (CTD-CNO) for managing the data. It is supported by grants from the French League Against Cancer (LNC) and the French National Cancer Institute (INCa). We thank the clinical research associates Chantal Rieux, Bérénice Legrand, Clotilde Pupin, Delphine Bridelance, and Loréna Masseline for data collection, as well as Bérengère de Gourmont for support with data entry. We acknowledge Ray Cooke for copyediting the manuscript. We also thank all patients who agreed to participate. The National Clinical Research Platform for Quality of Life in Oncology is labeled by the LNC.
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