The coronavirus disease 2019 (COVID-19) outbreak originated in Wuhan, China in late December 2019 and quickly escalated into a global pandemic (Liu et al., 2020; Zhu et al., 2020). While this has caused formidable disruption to the world population at scale, the psychological impact in vulnerable groups with pre-existing conditions calls for special attention. As a life-threatening disease, cancer increases the risk of developing mental health problems, including depression, anxiety, and distress (Mitchell et al., 2011; Inagaki et al., 2015; Ng et al., 2018). It is estimated that approximately one-third of cancer patients are affected by mental health disorders (Massie, 2004; Singer et al., 2010; Mitchell et al., 2011). Additionally, at the time of the study, it was unclear whether the effects of COVID-19 would be more severe in cancer patients. The general consensus is now that the mortality rate for infected cancer patients is significantly higher compared to the general population (Chen et al., 2020a; Gosain et al., 2020; Mehta et al., 2020). Thus, in a situation of health emergency, such as the one we are currently facing, these patients are likely to experience a trade-off between the increased risk of contracting COVID-19 when receiving cancer treatments and the increased risk of worsening cancer prognosis when postponing treatments (Burki, 2020). The present study explores the prevalence of COVID-19-related distress and anxiety in a population of Italian cancer patients.

A growing number of studies conducted during the COVID-19 pandemic have already highlighted mental health issues in the general population (Cuiya et al., 2020; Hossain et al., 2020a,b; Xiong et al., 2020). In Italy, one of the most severely hit countries in Europe in the first wave of the pandemic, several studies have explored the psychological impact of the pandemic using online and remotely administered surveys (Ferrucci et al., 2020; Mazza et al., 2020; Rossi et al., 2020; Brivio et al., 2021a). Three weeks into the national lockdown Rossi et al. (2020) found relatively high levels of adverse mental health outcomes among Italians, with 37% reporting post-traumatic stress symptoms (PTSS), 17% reporting depressive symptoms, and 21% reporting severe anxiety symptoms. Being a woman and younger age were associated with more severe psychological outcomes. Focusing on the COVID-19 pandemic as a traumatic event, partly worsened by media communication (Brivio et al., 2020), Brivio et al. (2021a) assessed PTSS and generalized anxiety in the months following the disease outbreak. An online survey was set up for this exploratory study and included the standardized Italian versions of the impact of event scale revised (IES-R) and the generalized anxiety scale (GAD-7), as well as socio-demographic questions to identify potential risk factors. Results revealed severe levels of PTSS and mild levels of anxiety in the general population and identified important gender and age differences. Specifically, younger respondents displayed higher levels of distress and anxiety than older respondents, and female respondents experienced greater distress and anxiety compared to males. This gender effect mirrors findings from other studies (Mazza et al., 2020; Rossi et al., 2020) and appears to be consistent with studies on the fear of COVID-19, where anxiety is observed to be higher in women (Evren et al., 2020; Soraci et al., 2020; Reznik et al., 2021).

COVID-19 has detrimental effects on the lives of cancer patients due to the uncertainty regarding treatment and screening, combined with the fear of being infected (Gregucci et al., 2020; Brivio et al., 2021b). Several studies have reported considerably high levels of anxiety, depression, and post-traumatic stress disorder (Beaty et al., 2018; Chen et al., 2020b, 2021; Sigorski et al., 2020; Swainston et al., 2020; Ayubi et al., 2021; Yasin, 2021), and increased emotional vulnerability (Pigozzi et al., 2021). In some cases, respondents were cancer patients undergoing treatment at the time of the study (Sigorski et al., 2020; Chen et al., 2021), but active treatment status was not always among the inclusion criteria (e.g., Swainston et al., 2020; Yasin, 2021). The vast majority of surveys were administered online and assessed patients’ psychological health (Chen et al., 2020b; Romito et al., 2020; Sigorski et al., 2020; Swainston et al., 2020; Yasin, 2021) and their fear of tumor progression (Chen et al., 2020b; Sigorski et al., 2020) during the first wave of the COVID-19 pandemic. Work from China revealed that among 6,213 cancer patients, 23.4% had depression, 17.7% had anxiety, and 9.3% had post-traumatic stress disorder (Wang et al., 2020). Compared with males, females had a higher frequency of worrying about disease management, higher psychological pressure, and lower sleep quality because of the pandemic. In Italy, Romito et al. (2020) used validated questionnaires of anxiety, depression, and PTSS in patients with lymphoma and found that 36% fulfilled the diagnostic criteria for anxiety, 31% for depression, and 36% scored above cutoff for PTSS. In line with other studies, women were found to be more vulnerable to both anxiety and PTSS (Dückers and Olff, 2017), while younger patients showed higher levels of PTSS, an effect which mirrors the one seen in healthy participants (Rossi et al., 2020; Brivio et al., 2021a).

At present, only a handful of studies have directly compared the psychological effects of the pandemic on cancer patients and healthy controls, and the evidence is not always consistent (Musche et al., 2020; Ng et al., 2020). Here we contrasted the levels of anxiety and PTSS in cancer patients and healthy participants using two standardized tools, namely, the Generalized Anxiety Disorder (GAD-7) and the Impact of Event Scale revised (IES-R). Building on the literature showing an increased risk of anxiety symptoms and stress in women in both cancer (Romito et al., 2020; Sigorski et al., 2020) and healthy populations (Dückers and Olff, 2017; Rossi et al., 2020; Brivio et al., 2021a), this investigation focused on a female sample. Disruption to treatment and screening was also considered, given previous evidence of higher emotional vulnerability in women who experienced disruptions to scheduled oncology services (Swainston et al., 2020). The aim of the present study was twofold. First, we aimed to compare the prevalence of generalized anxiety and PTSS between cancer patients and healthy respondents in Italy, in the months following the outbreak. Given the additional burden that patients with cancer are experiencing, we expected to find higher adverse psychological outcomes in patients compared to healthy participants that are matched by socio-demographic variables. To our knowledge, this is the first study to investigate the topic in Italian cancer patients using a differential design. Second, having established the extent of the psychological impact of the pandemic on cancer patients, the study further examined if socio-demographic variables which have previously been correlated to psychological outcomes in the general public might be associated with psychological adverse events in our cancer population.

Feelings of anxiety and distress are a common feature of situations of uncertainty, of which the COVID-19 pandemic is a recent example. While the health crisis has affected mental health globally, cancer patients are more likely to experience contrasting emotional states, battling between the need to continue life-saving medical procedures and the fear of exposing themselves to the virus. The present study investigated the psychological burden of cancer patients in Italy in the months following the outbreak. We contrasted psychological outcomes in a sample of cancer patients and a group of healthy respondents matched for age and education using the same validated measures of generalized anxiety and PTSS. Results revealed higher levels of anxiety and PTSS in patients compared to healthy participants. In the cancer population, several clinical and demographic variables were found to affect the probability of developing adverse mental health outcomes. In particular, younger patients experienced higher levels of hyperarousal and anxiety compared to older patients, while respondents with children had more frequent intrusions than those without children. The impossibility to attend regular medical visits throughout the lockdown was found to be a risk factor, with patients whose appointments were postponed experiencing higher levels of PTSS and anxiety. Overall, these findings are in line with previous evidence collected during the pandemic and highlight the importance of monitoring mental health in vulnerable cancer populations.

While control groups of healthy respondents have sometimes been used in similar studies, the evidence is scarce and not always consistent. For example, Musche et al. (2020) showed comparable levels of distress and general anxiety in treated cancer patients relative to healthy controls. Another study found low levels of psychological distress and anxiety in both cancer survivors and healthy controls, with significantly lower levels of distress in the cancer population (Ng et al., 2020). Such pattern of results might be explained in terms of more effective coping strategies in cancer patients, who have learned to deal with stressful situations effectively (Livneh, 2000), but they may also be indicative of a low psychological distress and anxiety across groups. In contrast, our study showed elevated levels of distress and anxiety in response to the health emergency. This difference may be partially due to the way communication was initially managed at mass level during the first wave of COVID-19 (Brivio et al., 2020), when the risk of infection in Italy was profoundly different from that experienced in other European countries, where the other studies were conducted.

In this framework, the novel findings that oncological patients experienced more severe PTSS and anxiety than healthy participants can be explained assuming the COVID-19 pandemic as a source of trauma that would particularly affect individuals who are already physically and psychologically vulnerable due to cancer (Miaskowski et al., 2020). In this context, adverse mental health outcomes may be the result of overthinking about their safety and feeling in danger of contracting the virus, because of their physical debilitation and a reduced immune response due to cancer treatments. Future studies could explore associations between the subjective level of information about COVID 19 and adverse mental health outcomes, as high levels of information may reduce the psychological burden experienced by patients and level down differences with the healthy population (Musche et al., 2020).

Unlike previous studies which have assessed PTSS using the IES-R total sum score (Fiorillo and Gorwood, 2020; Romito et al., 2020; Wang et al., 2020; Joly et al., 2021), here we focused on the different sub-dimensions of post-traumatic stress disorder. This becomes interesting in the exploration of socio-demographic and clinical variables associated with negative mental health outcomes in cancer patients (Oliveri et al., 2019). We showed that younger respondents (aged 26–40) experienced more hyperarousal symptoms and anxiety than older patients (aged 56–75). These results replicate recent evidence by Brivio et al. (2021a) and are consistent with previous literature showing that younger age groups tend to have higher levels of PTSS than senior respondents (Ozamiz-Etxebarria et al., 2020; Romito et al., 2020), and experience greater cancer-related distress compared to older patients (Burgoyne et al., 2015). During the pandemic, this group had to delay major life milestones, such as buying a home, planning a family, or making a career move. We should also consider that many women diagnosed with cancer undergo treatment while negotiating work and family responsibilities, and this is particularly true for women belonging to generation Y. Nevertheless, the age difference could also be suggestive of a life span pattern of distress, whereby distress decreases with age independently of cancer or other chronic illnesses (Chittleborough et al., 2011). Among the socio-demographic variables examined, parental status was also associated with PTSS. Specifically, patients with children had more frequent intrusions compared to patients without children, possibly reflecting a heightened sense of responsibility toward the family in the event of contracting the disease. This result resonates with research showing greater chance of developing anxiety and depression in cancer patients with children as compared to similarly ill patients without cancer (Nilsson et al., 2009).

Additionally, analyses of the dimensions of IES-R showed that having to pause medical visits caused a significant increase in PTSS and anxiety. While we did not differentiate between cancer types in our study, future research should explore whether specific cancers (i.e., those with a faster progression rate) may be associated with different levels of anxiety and PTSS. Nevertheless, this finding is consistent with the literature (Swainston et al., 2020) and suggests that patients fear the consequences associated with interrupting their regular contacts with the hospital. Such insights are relevant for the management of hospital distress related to the COVID-19 pandemic, with psychological interventions becoming core components of cancer care protocols (De Berardinis et al., 2021). Future studies could also explore the psychological impact that COVID-19 pandemic had on patients who were undergoing different types of therapies (e.g., chemotherapy, radiotherapy, immunotherapy, and adjuvant hormone therapy) to explore differences in distress levels and specific needs.

A final consideration concerns previously documented gender differences in mental health, where mounting evidence suggests that women are more vulnerable to anxiety and distress. In a recent study, Brivio et al. (2021a) found higher levels of stress during the COVID-19 pandemic in female compared to male participants, replicating similar studies (Pappa et al., 2020; Vindegaard and Benros, 2020). Here we focused on female cancer patients, who are more likely to suffer the psychological burden of COVID-19. Nevertheless, our direct comparison of cancer and non-cancer patients allowed us to isolate the effect of being a female cancer patient during the pandemic. A large number of women have lost their job, been put on leave, or have reduced their hours due to the pandemic, causing financial stress that amplified the level of distress generated by the life-threatening disease (Simha et al., 2020). Future studies could explore interactions between gender and clinical interventions aimed at reducing COVID-19-related anxiety.

The primary strength of this study is that the empirical evidence used to compare the two populations was generated using the same standardized measures, allowing for direct comparison of results. The observation that patients with cancer experience more adverse mental health outcomes stresses the importance of providing continuity of care throughout future waves of the pandemic, and highlights the role of a clear and honest communication about the strategies to mitigate contagion risks. This study also had some limitations. First, the generalizability of the results is limited by the sampling technique adopted, which may have introduced biases in the sample composition. Second, the surveys were administered online, with respondents being given instructions as to how to complete the survey. While this gave us the possibility of reaching a wider geographical area, a general limitation of online research is the lack of control over who is completing the survey. It is unclear whether respondents received help when completing the survey, and how this may have influenced their answers.

In conclusion, this research highlights the importance of providing psychological interventions and support to cancer patients in pandemic times. With technology advancing at unprecedented rates, e-health applications could be used as valid alternative to guarantee a continuous communication with patients. This may be particularly beneficial for younger generations, who are not only the ones experiencing higher distress and anxiety, but also those who may be more favorable to digital medicine. Further research is required to identify the most effective channels and devices.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The studies involving human participants were reviewed and approved by the European Institute of Oncology Ethical Committee. The patients/participants provided their written informed consent to participate in this study.

EB, SO, PG, KM, and GP contributed to conception and design of the study. LL, EB, and MC organized the database and performed the statistical analysis. LL wrote the initial draft of the manuscript and revised the drafts during peer-review. GP supervised the study. All authors contributed to the article and approved the submitted version.

EB is supported by a personal grant from Fondazione Umberto Veronesi.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.