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. 2022 Oct 28;31(6):e13762. doi: 10.1111/ecc.13762

The psychological impact of COVID‐19 among newly diagnosed patients with breast cancer when cancer care was returning to normal

Jie Li 1,2, Songying Zhu 3, Wei Gao 3,✉
PMCID: PMC9874744  PMID: 36307937

Abstract

Objective

We aim to evaluate anxiety, depression and fear of cancer progression in newly diagnosed patients with breast cancer when cancer care was returning to normal after COVID‐19 by comparing them with the pre‐COVID patients and explore the association of worries about further cancer care and loneliness with them.

Methods

Two hundred and eighteen newly diagnosed patients with breast cancer during the pandemic were surveyed using questionnaires, and 153 patients before the pandemic were included in the control group. Logistic regression analyses were used.

Results

There were 51.8%, 44.0% and 30.7% of patients during the pandemic reported anxiety symptoms, depressive symptoms and clinically significant fear of cancer progression, respectively. The risks of anxiety symptoms (OR 2.24, 95% CI 1.43–3.51), depressive symptoms (1.61, 1.04–2.50) and clinically significant fear of cancer progression (4.65, 2.49–8.70) were higher in patients during the pandemic than pre‐COVID patients. Worries about further cancer care and loneliness were associated with 1.40–2.52 times higher risks of these psychological problems among the patients during the pandemic.

Conclusions

The newly diagnosed patients with breast cancer during COVID‐19 are at elevated risks of depression, anxiety and fear of cancer progression, and those who are worried about further cancer care and felt loneliness during the pandemic were more likely to experience psychological problems.

Keywords: anxiety, breast cancer, COVID‐19, depression, fear of cancer progression, fear of cancer recurrence

1. BACKGROUND

The coronavirus disease 2019 (COVID‐19) pandemic threatened people's physical health and also impacted their mental health (Cenat et al., 2021; Liu et al., 2020). It has been evidenced as a traumatic stressor and can cause mental health problems, such as posttraumatic stress disorder, anxiety and depression in general populations (Bridgland et al., 2021). Breast cancer impacts a large number of women as it was the most prevalent female cancer with an estimated incidence of 47.8/100,000 around the world (Sung et al., 2021). Patients with cancer have been considered a vulnerable population during the pandemic (Gov.UK, 2020). Those patients with breast cancer may perceive more psychological stress during the COVID‐19 pandemic as women were found to be more sensitive to psychological stress (Sze & Brunton, 2020). Combined with the stress of the diagnosis and treatment of breast cancer, patients with breast cancer may be at a higher risk of experiencing psychological problems during the pandemic.

In a qualitative study of breast cancer patients undergoing treatment, the patients reported increased psychological distress and worries, such as a higher risk of catching COVID‐19, changes in cancer care and decreased family relationships (Savard et al., 2021). Quantitative studies found that the prevalence of symptoms of anxiety was 18.2%–67.7% (Chen et al., 2021; Cui et al., 2020; Juanjuan et al., 2020; Kim & Kim, 2022; Massicotte et al., 2021; Mink van der Molen et al., 2021) and depressive symptoms were 16.0%–53.0% (Chen et al., 2021; Cui et al., 2020; Juanjuan et al., 2020; Kim & Kim, 2022; Massicotte et al., 2021; Mink van der Molen et al., 2021) among patients with breast cancer during the COVID‐19 pandemic, which were much higher than the prevalence of symptoms of anxiety and depression in the general population during the pandemic (Cenat et al., 2021; Lakhan et al., 2020; Salari et al., 2020). Besides increased anxiety and depression, patients with breast cancer also experience high levels of fear of cancer progression (Kim & Kim, 2022; Koral & Cirak, 2021; Massicotte et al., 2021; Soriano et al., 2021; Xie et al., 2021). However, most of the previous studies were conducted in the outbreak stage of the pandemic (from January to April 2020), with few focused on the psychological problems of the patients later in the relatively stable stage of the pandemic. At that time, although cancer care service in the hospital was back to normal, there were still differences from the pre‐COVID period because of the protective measures of COVID‐19 (e.g., limitation of the amount of hospitalised patients, permitting only one caregiver in the inpatient wards and no other visitors). Moreover, in most of the previous studies, symptoms of anxiety, depressive symptoms and fear of cancer progression/recurrence of the patients were assessed only during the pandemic, with no comparisons with the patients before the pandemic, except for limited longitudinal studies from before to during the COVID‐19 pandemic (Bargon et al., 2021; Rentscher et al., 2021). The two longitudinal studies found that levels of depression and anxiety were higher in patients during the pandemic than the patients before the pandemic, but fear of cancer progression was not evaluated. A comparison with the patients of a similar background before the pandemic will help to illustrate whether and to what extent the patients during the pandemic experienced increased symptoms of anxiety, depression and fear of cancer progression.

The pandemic has brought about changes in cancer care and also affect feelings of the patients with breast cancer, for example, worries about further reexamination and treatment and feelings of loneliness (Bargon et al., 2021; Papautsky & Hamlish, 2021; Rentscher et al., 2021; Savard et al., 2021). More than half of the patients reported delays in cancer treatment, and nearly half of the patients with breast cancer reported fear about that the COVID‐19 pandemic would impact their delays in accessing cancer care or recovery (Hamlish & Papautsky, 2022; Ludwigson et al., 2022; Xie et al., 2021). These would induce the patients' psychological problems like depression and anxiety, which has been evidenced in cancer patients (Eckford et al., 2021) and noncancer populations (Lambert et al., 2022; Liu et al., 2020). For patients who were newly diagnosed with breast cancer and just started the treatment, they were more likely to worry about whether future scheduled treatment will be on time (Booth et al., 2005). The uncertainty of the pandemic increased the worry, which may result in elevated levels of anxiety and depression, as well as fear of cancer progression (Soriano et al., 2021). More evidence was needed to clarify the association between the pandemic‐related changes and psychological problems among patients with breast cancer.

The purposes of the current study were to evaluate anxiety, depression and fear of cancer progression in newly diagnosed patients with breast cancer during the COVID‐19 pandemic by comparing them with the patients in pre‐COVID time and explore the association between the pandemic‐related factors (worries about further cancer care and loneliness because of the pandemic) and these psychological problems. We hypothesized that the patients with breast cancer would be at higher risks of anxiety, depression and fear of cancer progression than their counterparts before the pandemic, and among patients during the pandemic, worries and loneliness were associated with higher risks of psychological problems.

2. METHODS

2.1. Participants

Patients with breast cancer who were hospitalised at the Department of Breast Surgery between July and October 2020 were recruited. The inclusion criteria were aged ≥18 years, first diagnosed with breast cancer, in Stage I–III, completed surgery treatment for breast cancer within 1 week and had sufficient Chinese language skills to understand and complete the survey. Patients who had a history of psychiatric disorders, cancer or anticancer treatment were excluded. Two hundred and eighteen patients completed the survey. The patients before the pandemic (control group) were from our previous survey investigating the psychological status among newly diagnosed patients with breast cancer between July and November 2019. One hundred and fifty‐three patients were included in the control group according to the inclusion and exclusion criteria of this study.

2.2. Measures and data collection

Depressive symptoms were assessed using the Chinese version of the 9‐item depression module from the Patient Health Questionnaire (PHQ‐9) (Kroenke et al., 2001). Responses for each item were 0 (not at all), 1 (several days), 2 (more than half the days) and 3 (nearly every day). The total score ranges from 0 to 27, and a higher score indicates severer symptoms of depression. The cutoff score for depressive symptoms was ≥5 (Kroenke et al., 2001). The Chinese version has good reliability and validity (Wang et al., 2014). The Cronbach's alpha coefficient in the current study was 0.902.

The 7‐item Generalised Anxiety Disorder Scale (GAD‐7) was used to measure symptoms of anxiety (Spitzer et al., 2006). Each item is rated on a 4‐Likert scale ranging from 0 (not at all) to 3 (nearly every day). A total score ≥5 was used as the cutoff criterion for anxiety symptoms (Spitzer et al., 2006). The Chinese version has been shown to be a reliable and valid measure for symptoms of anxiety (Zeng et al., 2013). The Cronbach's alpha coefficient in the current study was 0.915.

The 12‐item Fear of Progression Questionnaire (FoP‐12) was used to assess the fear of cancer progression of the patients (Mehnert et al., 2009). The items are rated on a 5‐Likert scale, ranging from 1 (never) to 5 (very often). The total score ranges from 12 to 60; a higher score indicated a higher level of fear. A total score of ≥34 was used to determine clinically significant fear of cancer progression (Herschbach et al., 2010; Sarkar et al., 2014). The Chinese version of the FoP‐12 showed good reliability and validity (Mahendran et al., 2020). The Cronbach's alpha coefficient in the current study was 0.916.

Demographic characteristics related to age, education, marital status, employment status and family monthly income were collected by self‐reported questions. Information on the cancer stage was collected from medical records. Additional questions were developed to evaluate the worries and loneliness brought by the pandemic, including ‘Are you worried that further cancer care (e.g., reexamination and treatment) would be interrupted by the COVID‐19?’ and ‘Did you feel loneliness when you were at home because of the COVID‐19?’

Two nurses working in the department were trained as the investigators of the survey. They found the eligible participants by reviewing the medical records and then the eligible patients who agreed to participate completed the survey. Ethics approval was obtained from the School of Public Health, Shandong University (No. LL20200701).

2.3. Statistical analysis

Frequencies (proportions), means (standard deviations) and medians (interquartile ranges) were used to describe the variables. A two independent samples t‐test for age and a χ 2 test for categorical variables were used to examine differences in characteristics between patients during and before COVID‐19. A Mann–Whitney U test and a χ 2 test were used to examine group differences in the levels and prevalence of anxiety and depressive symptoms and fear of cancer progression. The association between COVID‐19 experience and anxiety, depression and fear of cancer progression was tested using logistic regression analyses. Age, education and other characteristics, which were different between groups with a p‐value <0.1 of the χ 2 test, were included in logistic regression models to adjust for potential confounders. Logistic analyses were also used to explore the association of worries and loneliness with the psychological problems among patients during the pandemic, controlling the sample characteristics. Statistical analyses were performed using IBM SPSS, version 24.0 (IBM Corp., Armonk, NY, USA). A two‐sided p‐value less than 0.05 was considered statistically significant.

3. RESULTS

3.1. Sample characteristics

Table 1 shows descriptive statistics of the participants' characteristics. The patients during the pandemic were on average 52.32 (SD = 11.14) years of age, ranging in age between 20 and 81 years. Most (96.3%) of them were married. About half of them had at least a middle school education (47.2%), Stage I of breast cancer (50.9%) and frequency of physical activity more than three times per week (46.8%). There were no significant differences in age, marital status and TNM stages between patients during and before the pandemic. There were fewer percentages of the patients during the pandemic having education of ≥middle school and being employed than the patients before the pandemic.

TABLE 1.

Characteristics of the patients with breast cancer during and before COVID‐19

Characteristics During COVID‐19 (n = 218) Before COVID‐19 (n = 153) χ 2/t p
Age, mean ± SD 52.32 ± 11.14 51.08 ± 11.87 −1.03 0.304
Education 8.27 0.004
<Middle school 115 (52.8) 59 (38.6)
≥Middle school 103 (47.2) 94 (61.4)
Employment 8.27 0.004
Unemployed 158 (72.5) 89 (58.2)
Employed 60 (27.5) 64 (41.8)
Marital status 0.02 0.900
Married 210 (96.3) 147 (96.1)
Not married/widowed 8 (3.7) 6 (3.9)
Family monthly income
≤¥3000 115 (52.8) –
>¥3000 103 (47.2) –
Physical activity
≤3 times/week 116 (53.2) –
>3 times/week 102 (46.8) –
TNM stages 3.43 0.064
I 111 (50.9) 63 (41.2)
II–III 107 (49.1) 90 (58.8)
Worries about further cancer care
Yes 96 (44.0) –
No 122 (56.0) –
Feeling loneliness
Yes 78 (35.8) –
No 140 (64.2) –
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Abbreviation: COVID‐19, coronavirus disease 2019.

3.2. Comparisons of anxiety, depression and fear of cancer progression between patients during and before the COVID‐19 pandemic

The levels of anxiety, depression and fear of cancer progression were higher in the patients during the pandemic than in the patients before the pandemic. The differences in anxiety and fear of cancer progression were significant, while the differences in depression were marginally significant. The prevalence of symptoms of anxiety, symptoms of depression and clinically significant fear of cancer progression was 51.8%, 44.0% and 30.7% in patients during the pandemic, respectively. Among them, the prevalence of anxiety and clinically significant fear of cancer progression was significantly higher than the patients before the pandemic. See Table 2.

TABLE 2.

Comparisons of anxiety, depression and fear of cancer progression between patients with breast cancer during and before COVID‐19

During COVID‐19 (n = 218) Before COVID‐19 (n = 153) χ 2/t p
Anxiety
GAD‐7 scores 5 (1, 7) 3 (0, 6) 3.93 <0.001
Symptoms of anxiety (≥5) 51.8% (113/218) 36.6% (56/153) 8.41 0.004
Depression
PHQ‐9 scores 4 (1, 8) 3 (5, 6) 1.84 0.066
Symptoms of depression (≥5) 44.0% (96/218) 35.3% (54/153) 2.85 0.091
Fear of cancer progression
FoP‐12 scores 27.91 ± 10.19 21.44 ± 8.64 6.59 <0.001
Clinically significant fear of cancer progression (≥34) 30.7% (67/218) 9.8% (15/153) 22.87 <0.001
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Abbreviations: COVID‐19, coronavirus disease 2019; FoP‐12, the 12‐item Fear of Progression Questionnaire; GAD‐7, the 7‐item Generalised Anxiety Disorder Scale; PHQ‐9, the 9‐item depression module from the Patient Health Questionnaire.

3.3. Association between COVID‐19 experience and anxiety, depression and fear of cancer progression

After controlling for age, education, employment and cancer stages, patients with breast cancer during the pandemic were 1.24 times (OR 2.24, 95% CI 1.43–3.51), 0.61 times (1.61, 1.04–2.50) and 3.65 times (4.65, 2.49–8.70) more likely to experience symptoms of anxiety, depressive symptoms and clinically significant fear of cancer progression (Table 3).

TABLE 3.

Logistic regression analyses for the association between COVID‐19 experience and anxiety, depression and fear of cancer progression (n = 371)

Anxiety symptoms OR (95% CI) Depressive symptoms OR (95% CI) Clinically significant fear of cancer progression OR (95% CI)
COVID‐19 experience
No 1.00 1.00 1.00
Yes 2.24 (1.43–3.51)*** 1.61 (1.04–2.50)* 4.65 (2.49–8.70)***
Controlled variables
Age 0.98 (0.96–1.00) 1.00 (0.98–1.02) 0.99 (0.97–1.02)
Education
<Middle school 1.00 1.00 1.00
≥Middle school 1.21 (0.75–1.95) 1.22 (0.76–1.96) 1.19 (0.67–2.10)
Employment
Unemployed 1.00 1.00 1.00
Employed 1.04 (0.60–1.79) 1.27 (0.74–2.17) 1.31 (0.69–2.52)
Cancer stages
I 1.00 1.00 1.00
II–III 2.55 (1.63–3.99)*** 1.48 (0.96–2.29) 1.43 (0.84–2.43)
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Abbreviation: COVID‐19, coronavirus disease 2019.

*

p‐value <0.05.

***

p‐value <0.001.

3.4. Association of COVID‐19 related worries and loneliness with anxiety, depression and fear of cancer progression

There were 44.0% (96/218) of the patients during the COVID‐19 reported worries about further cancer care and 35.8% (78/218) reported loneliness (Table 1). As shown in Table 4, patients who were worried that further cancer care would be interrupted by the pandemic were 1.70 times (OR 2.70, 95% CI 1.48–4.93), 1.40 times (2.40, 1.34–4.29) and 1.56 times (2.56, 1.37–4.78) more likely to report symptoms of anxiety, depressive symptoms and clinically significant fear of cancer progression, respectively; patients with the feeling of loneliness were 2.52 times (3.52, 1.86–6.67), 1.86 times (2.86, 1.56–5.22) and 1.70 times (2.70, 1.43–5.10) more likely to experience symptoms of anxiety, depressive symptoms and clinically significant fear of cancer progression, respectively (Table 4).

TABLE 4.

Logistic regression analyses for the association of worries about further cancer care and loneliness with anxiety, depression and fear of cancer progression in patients with breast cancer during COVID‐19 (n = 218)

Anxiety symptoms OR (95% CI) Depressive symptoms OR (95% CI) Clinically significant fear of cancer progression OR (95% CI)
Worries about further cancer care
No 1.00 1.00 1.00
Yes 2.70 (1.48–4.93)** 2.40 (1.34–4.29)** 2.56 (1.37–4.78)**
Feeling loneliness
No 1.00 1.00 1.00
Yes 3.52 (1.86–6.67)*** 2.86 (1.56–5.22)** 2.70 (1.43–5.10)*
Controlled variables
Age 0.98 (0.95–1.01) 1.00 (0.97–1.03) 0.99 (0.96–1.02)
Education
<Middle school 1.00 1.00 1.00
≥Middle school 1.03 (0.50–2.13) 0.95 (0.47–1.90) 1.22 (0.58–2.58)
Employment
Unemployed 1.00 1.00 1.00
Employed 1.30 (0.57–2.95) 1.23 (0.56–2.72) 1.27 (0.55–2.94)
Marital status
Married 1.00 1.00 1.00
Not married/widowed 0.55 (0.10–3.10) 0.45 (0.07–2.70) 0.87 (0.14–5.31)
Family monthly income
≤¥3000 1.00 1.00 1.00
>¥3000 0.94 (0.47–1.88) 0.94 (0.48–1.84) 0.60 (0.29–1.24)
Physical activity
≤3 times/week 1.00 1.00 1.00
>3 times/week 0.68 (0.37–1.26) 0.60 (0.33–1.10) 0.50 (0.26–0.97)*
TNM stages
I 1.00 1.00 1.00
II–III 2.09 (1.13–3.88)* 1.25 (0.69–2.27) 0.89 (0.46–1.69)
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Abbreviation: COVID‐19, coronavirus disease 2019.

*

p‐value <0.05.

**

p‐value <0.01.

***

p‐value <0.001.

4. DISCUSSION

We examined psychological problems (anxiety, depression and fear of cancer progression) in newly diagnosed patients with breast cancer during the COVID‐19 pandemic and explored the extent of the increased risks in patients during the pandemic compared with the patients before the pandemic. Results showed that 7 months following the outbreak of COVID‐19, 51.8% of the patients with breast cancer reported symptoms of anxiety, 44.0% reported depressive symptoms and 30.7% reported clinically significant fear of cancer progression. The risks of anxiety, depression and clinically significant fear of cancer progression in patients during the pandemic were significantly higher than the risks of the patients before the pandemic. In addition, we found an association between worries about further cancer care and loneliness with higher risks of psychological problems.

There were 51.8% and 44.0% of patients during the pandemic reported symptoms of anxiety and depression, respectively. In previous studies, the prevalence of anxiety symptoms in patients with breast cancer during the COVID‐19 pandemic ranged from 18.2% to 67.7% and 16.0% to 53.0% for depressive symptoms (Chen et al., 2021; Cui et al., 2020; Juanjuan at al., 2020; Kim & Kim, 2022; Massicotte et al., 2021; Mink van der Molen et al., 2021). The variety of the prevalence may result from the different criteria used to define anxiety and depressive symptoms and the different treatment stages of the patients. Three studies used the same classification as the current study found a prevalence of 56.2%–67.7% of anxiety symptoms and a prevalence of 47.3%–53.0% of depressive symptoms in patients with breast cancer (Chen et al., 2021; Cui et al., 2020; Juanjuan et al., 2020), slightly higher than the prevalence in our study. One of the possible reasons may be that most of them were under active treatment and experiencing therapy interruption because of the lockdown of the pandemic when they were evaluated, which may increase their anxiety and depression. Meanwhile, participants in the current study have been in hospital for treatment as the medical activities were back to normal at that time.

However, there were still more than half of the patients experienced anxiety symptoms, which was higher than their counterparts before the pandemic found in our study (36.6%) and previous studies (26.6%–42.4%) (Hashemi et al., 2020; Ju et al., 2018; Li et al., 2021). Compared with the patients before the pandemic, the patients during the pandemic were 1.24 times more likely to experience symptoms of anxiety in the current study. It may result from their worries about the interruption of future treatment as the great uncertainty of the pandemic (Mink van der Molen et al., 2021; Savard et al., 2021), which was also evidenced in our study. Since intolerance of uncertainty over the COVID‐19 pandemic has been shown to be related to elevated levels of anxiety and depressive symptoms (Wagener et al., 2022). In this study, the prevalence of symptoms of depression was marginally significantly higher in patients during the pandemic than those before the pandemic, and the extent of elevated risks was smaller than the elevated risk of anxiety. It was in line with the finding that the effect of intolerance of uncertainty on depressive symptoms was smaller than that on anxiety (Wagener et al., 2022).

There were 30.7% of patients with breast cancer reported clinically significant fear of cancer progression, and it was higher than the proportion in patients before the pandemic (9.8%). In a study using the same criteria of clinically significant fear of cancer progression among patients with breast cancer referred to radiation therapy in the early stage of the pandemic, the prevalence was 17.2% (Xie et al., 2021), which was lower than the patients during the pandemic in our study. Furthermore, we found that patients during the pandemic were 3.65 times more likely to experience clinically significant fear of cancer progression than the patients before the pandemic. It indicated that the newly diagnosed patients with breast cancer during the pandemic were more likely to fear cancer progression during the pandemic. The results were in accordance with the fear of cancer recurrence model that various cancer‐related external cues would trigger fear of cancer progression (LeeLee‐Jones et al., 1997). Our study indicated that the pandemic, which widely affected daily life, could be treated as one of the external cues causing fear of cancer progression.

Nearly half of the patients worried about further cancer care even when they were treated in hospital and the pandemic was becoming stable, and about one third of them experienced loneliness during COVID‐19. In line with Eckford et al.'s (2021) findings in cancer patients, concerns about changes in health care brought by COVID‐19 induced over 1.4 times increased risks of anxiety and depression among patients with breast cancer. In addition to anxiety and depression, we also found an increased risk for fear of cancer progression by worries in patients with breast cancer. Loneliness was found to be associated with psychological problems such as anxiety and depression in patients with breast cancer before the pandemic (Fanakidou et al., 2018) and in young adults during COVID‐19 (Liu et al., 2020). A consistent finding was found among patients with breast cancer in the current study.

4.1. Study limitations

The present study was one of the first studies to demonstrate the extent of changes in common psychological problems, including anxiety, depression and fear of cancer progression, in the newly diagnosed patients with breast cancer during the COVID‐19 pandemic by comparing them with the patients with similar background before the pandemic. The results also indicate worries about further cancer care and loneliness as the risk factors for anxiety, depression and fear of cancer progression in the patients during the pandemic. However, several limitations should be acknowledged. First, patients during and before the pandemic were not fully balanced in their background characteristics, which may result in bias in the results. But some key variables such as age, marital status and TNM stages were not significantly different between the groups, and the discriminative factors were controlled in the logistic regression analyses to address the unbalance. Second, the results were limited to that anxiety, depression and fear of cancer progression were evaluated only among newly diagnosed patients after the surgery. Patients with longer disease duration and different treatment types should be considered in future studies to generalise the results to more patients. Finally, this study utilised a cross‐sectional design, which limited the clarity of the effect of worries and loneliness on the changes in psychological problems. Further research including follow‐up of psychological problems would help to reinforce our findings.

4.2. Conclusions and clinical implications

In conclusion, the newly diagnosed patients with breast cancer during the COVID‐19 pandemic are more likely to experience depression, anxiety and fear of cancer progression than those before the pandemic, with the highest increased risks in fear of cancer progression; worries about further cancer care and loneliness were associated with the elevated risks of these psychological problems in patients during the pandemic. Our results indicate the importance of psychological problems screening for newly diagnosed patients with breast cancer during the outbreak of a major infectious disease like COVID‐19. Interventions to reduce worries and loneliness may be taken into account to improve the mental health of the patients.

CONFLICTS OF INTEREST

The authors have no conflicts of interest to disclose.

ACKNOWLEDGEMENT

This research was supported by the National Natural Science Foundation of China (72004119).

Li, J. , Zhu, S. , & Gao, W. (2022). The psychological impact of COVID‐19 among newly diagnosed patients with breast cancer when cancer care was returning to normal. European Journal of Cancer Care, 31(6), e13762. 10.1111/ecc.13762

Funding information National Natural Science Foundation of China, Grant/Award Number: 72004119

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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