Introduction

The ongoing coronavirus (COVID-19) pandemic has led to a global public health response.1 In Australia, an increased burden on the healthcare system and resource needs resulted in non-urgent elective surgery being postponed from March 2020.2 In response to COVID-19 case numbers, there was varying easing and tightening of restrictions across the states and territories throughout the pandemic. These restrictions had an important impact on patients with thyroid cancer—the standard treatment for thyroid cancer is the surgical removal of part (hemithyroidectomy) or all (total thyroidectomy) of the thyroid, depending on the type of thyroid cancer and/or size of the tumour(s). Some surgeries for small thyroid cancers or diagnosis of thyroid cancer, such as hemithyroidectomy for atypical nodules, were delayed due to restrictions to operating capacity.3 While these restrictions did not affect the treatment of clinically urgent thyroid cancer cases, they potentially led to delays in diagnosis due to difficulty with healthcare access and restricted access to imaging procedures.4

Though most types of thyroid cancer have a high survival rate, the quality of life for these patients is of interest. One systematic review suggested that survivors of thyroid cancer tend to have similar or slightly poorer health-related quality of life than the normative population.5 Another study found that patients with differentiated thyroid cancer experience anxiousness related to the risk of recurrence and the risk of developing other types of cancer.6

While this is known about patients with thyroid cancer, our understanding of the impact of delays in treatment on patients with thyroid cancer is limited. Despite this, research has emerged on delays in other cancers, such as breast and prostate cancers during the COVID-19 pandemic.7 8 A recent study suggests that there is no significant association between surgical delays and adverse oncological outcomes or disease progression in medium-risk to high-risk patients with prostate cancer.7 However, another study looking at the psychosocial impact of delayed treatment on patients with breast or prostate cancer reported high levels of distress due to the combination of cancer-related and COVID-related worries.8 It is important to understand whether there are similar clinical and psychological outcomes for patients with thyroid cancer who experience unexpected delays to diagnosis and/or treatment. The findings of this study may also improve our understanding of how delayed thyroid cancer treatments can be clinically managed in the future.

MethodsStudy design

This study followed a thematic analysis research design, allowing for a descriptive and nuanced interpretation of the themes that emerged.9 Semi-structured qualitative telephone interviews were undertaken to understand the impact of delayed diagnosis and/or treatment of patients with thyroid cancer during COVID-19.

Sample and recruitment

Patients aged 18 years or older who were diagnosed with primary thyroid cancer and had delayed diagnosis and/or treatment due to the COVID-19 pandemic were eligible. Patients were eligible for the study if they had a diagnosis of thyroid cancer and any delay to their treatment, which could include a delay in diagnosis, delay in surgery or further treatment such as radioactive iodine treatment. Patients were excluded from the study if they were non-English speaking, or could not provide informed consent. Patients were recruited through key Australian and New Zealand Endocrine Surgeons members and clinicians, and through the Australia and New Zealand Thyroid Cancer Registry. Eligible patients were purposively identified and notified of the study by the clinicians and given an invitation letter, the Participant Information Statement and Expression of Interest form to return to the clinician or directly to the research team via email. Registry participants who were diagnosed with thyroid cancer from April to June 2020 from across Victoria and New South Wales were sent a mail-out invitation. Participants returned their expressions of interest and were screened via phone call to ascertain suitability for the study. Eligible patients were interviewed after providing written or oral consent. The participants did not receive a stipend for participation in this study. Recruitment continued until no new themes emerged.

Data collection

A semi-structured interview schedule (see online supplemental appendix A) was developed using an iterative process by a multidisciplinary team, including thyroid clinicians, public health researchers and health psychologists. The interview schedule included—pathway to diagnosis, diagnosis specifics, delay in treatment, initial views and attitudes towards delayed treatment, actual experiences of delayed treatment and retrospective reflection on the delayed treatment experience. The interviews were conducted via telephone by two researchers with training and experience in qualitative methods (BD and BN), audio-recorded and transcribed verbatim by an external transcription company. BD is a research student and BN is a public health researcher working in the area of cancer communication and decision-making. The interviews were conducted between June 2020 and October 2021 and ranged from 15 min to 43 min in duration, with a median interview duration of 23 min.

Patient and public involvement

The study was piloted and conducted in patients with thyroid cancer. The findings of this study have been summarised and disseminated to the participants.

Data analysis

The study methodology used thematic analysis, and the transcribed interviews were analysed using thematic framework analysis.10 The transcripts were analysed independently by the three researchers (BD, CB and BN) to identify codes that could be linked together by related concepts. The agreed-upon initial themes and concepts were then grouped into broader themes and subthemes. Following this, RHD read a subset of the transcripts to inform the final version of the coding framework. Two researchers (BD and BN) were involved in the coding process, where BD coded all the transcripts and BN double coded 20% of the transcripts in Microsoft Excel. On completion of the coding and double-coding, a table of quotes listed under themes and subthemes was circulated to the research team (AG, BN, LI) to finalise for inclusion. After this, the final results were reported using the Consolidated Criteria for Reporting Qualitative Research Publication Guidelines.11

Results

A total of 20 patients were interviewed (16 females and 4 males). Three patients were excluded from the analysis after being interviewed. These patients were unsure if they had experienced a delay in the screening process, and on completing the interviews it was determined that the patients had not experienced any delays. The 17 participants included in this study (14 females and 3 males) had a median age of 48 (range 35–77) years old (table 1). Most patients interviewed were treated in a private healthcare setting (table 2). The key emerging themes with supporting quotes from the interviews are detailed below, and a comprehensive overview of additional supporting quotes for each theme can be found in online supplemental appendix B.

Table 1

Demographics of study participants

Table 2

Treatment characteristics of study participants

Delays in diagnosis pathway

Some patients initially presented to their general practitioner for non-thyroid problems, while others presented with physical symptoms (e.g., sore throat, enlarged lymph node). Most patients were then diagnosed by a thyroid clinician (table 2). Many patients noted feeling worried about their diagnosis; however, patients who felt that they better understood their diagnosis expressed less concern.

Patients noted a variety of reasons for delays to diagnosis, including delays in fine needle aspiration cytology, as well as delays between diagnostic testing and seeing a thyroid clinician. One patient noted that their diagnosis was delayed due to difficulties getting a flight back to Australia during the pandemic. Another patient noted they put off their ultrasound due to COVID-19 and conflicting personal demands during the pandemic.

I didn’t go because it wasn’t anything that seemed to have any urgency about it and, because in that early stage in 2020, it was only to go and see the doctor or whatever for things that were serious or urgent. (3–6 months delay)

Initial management

Most patients were recommended to undergo surgery by their thyroid clinician, although one patient noted that active surveillance was discussed. Most patients trusted the management advice provided by their clinician. A sense of urgency was conveyed to some patients regarding their treatment.

What I was anxious about was that COVID was going to slow and delay things. I was reading articles about delaying elective surgery and because I’m not medical, I didn’t know the difference. (<3 months delay)

One patient noted that they were treated in a private setting as their treating clinician was concerned about the delays COVID-19 could have in the public sector.

…any other year, [the surgeon] would have said just wait and go through the public system but [the surgeon] does [their] surgery through the public system and it wouldn’t have been that long, but because [they] could see the pandemic coming, [they] said that [they] recommended I went private. (3–6 months delay)

Delay in management

Delays were primarily communicated to patients by a thyroid clinician, with most delays being communicated via telehealth, including telephone or video conferencing. While some patients accepted the news of the delay, others expressed worry towards disease progression and going to the hospital during the pandemic.

Initial views and experiences of delay

The patients’ feelings towards the delay initially included disappointment, anxiousness, anger and fear, though most patients understood that the delay was out of their control. Many of the patients interviewed experienced heightened emotional responses during the pandemic.

…I don’t how much my feeling is different to just anybody that’s been through the pandemic. But I really have felt a lot more fragile than previous years. (3–6 months delay)

One patient noted that they chose to delay their radioactive iodine treatment due to fears of being in a hospital setting at the height of the pandemic. Numerous patients expressed concerns about going to hospitals or health settings during the pandemic. Notably, most patients were treated through the private healthcare system (table 2), with some choosing private treatment over public in light of increased waiting times anticipated by the clinicians in the public sector.

During COVID like you don’t feel safe to go anywhere. (>6 months delay)

Others avoided further follow-up due to COVID-19 restrictions.

I was very aware at different times of worrying about it, and worrying about whether or not I really needed to do something or go and have this investigatory scan in the middle of a nation-wide lockdown, when everyone’s been told ‘unless it’s urgent, stay away’… (3–6 months delay)

Some patients were advised that treatment would recommence in 1 to 3 months, but this was mostly an estimate of what was ultimately unknown to healthcare providers. Most patients were supported by immediate family during this time, although COVID-19 restrictions did impact hospital visitation and the ability to access some healthcare facilities.

…you didn’t necessarily have the support of your family there. You know, my husband wasn’t able to attend the appointment with me, initially. (<3 months delay)

Views and experiences during delay

The patients reported numerous perceived impacts of COVID-19 on the care they received. Most patients noted slowed management and reduced communication with treating clinicians, as well as barriers to communication with the healthcare professionals. Some patients also reported the inability to access a nearby clinician in person and a lack of understanding of the information conveyed by the thyroid clinicians.

[The surgeon] just told me, ‘You have thyroid cancer’ but [the surgeon] didn’t explain. (<3 months delay)

One patient noted that they were regularly followed up and kept informed by their clinician. The majority of patients reported anxiousness towards their delayed treatment, with one patient noting that they felt they received little reassurance from their clinician during this time. Almost half of the patients interviewed expressed concerns regarding disease progression or tumour growth during their delay.

I always wonder[ed] whether the cancer grew in that time, the two-month delay. (<3 months delay)

You do wonder whether the delay has caused that, you know, that things have grown while I’ve been waiting. (<3 months delay)

Views and experiences after delay

Most patients accepted the need to have their treatment rescheduled. Though most understood the barriers to treatment due to the pandemic, some wondered if their disease would have been as invasive without the aforementioned delays.

…you know, if we had taken more action in February, would I be in the position I’m in now? Probably still would have been thyroid cancer but would it have been as invasive? (<3 months delay)

Some patients reported a significant financial burden as a result of being treated through the private healthcare system.

…I decided to go through private because COVID was hitting and I just felt very anxious. …I think it ended up costing about $20 000 through private. (<3 months delay)

…it did cost us a lot of money to have it done because I’d only just cancelled my private health insurance, you know, “I don’t need this anymore” and I couldn’t go public because the hospital, they had a lot of COVID patients in there so they weren’t accepting any surgeries in there. So yes, we were out of pocket a bit of money having to go with that private option but it was worth it. (<3 months delay)

The majority of patients were satisfied with their treating teams; however, a few noted that improved communication with their clinicians would have been appreciated. Almost all patients expressed that they did not want to wait any longer than they did if they had to experience similar delays again, with anxiousness and unease being the main influencing factors for their opinions.

…I was glad that it was done within that 2 months. I think it was because I didn’t know what it was. That was really concerning. So dragging that on would have increased my anxiety. (<3 months delay)

Discussion

Although concerns about cancer treatment are not unique to COVID-19, the findings of this study suggest that the pandemic may have increased the fragility and unease experienced by patients with thyroid cancer, including hesitancy about going to the hospital during this time.12 The interviews highlighted patients’ worries and concerns around the delayed treatment during COVID-19, especially uncertainty surrounding when surgery and other treatments would resume. Although this may be evident without the pandemic, it is clear that patients with thyroid cancer may not be comfortable delaying treatment.13 However, it was also found that some patients were accepting the delays as they felt it was largely out of their control.

There were notable changes in the management of patients during the COVID-19 pandemic. A higher proportion of the patients interviewed were treated through the private healthcare system compared with those treated through the public system (table 2), with one patient reporting a greater financial burden due to being treated privately, rather than in the public healthcare system.14 Telehealth became the primary means of communication between patients and clinicians and provided flexible approaches to providing patient care throughout the pandemic.15 16 However, its limitations include an inability to have physical examinations and a potential impact on communication.17 Barriers to seeing doctors in person throughout the pandemic, due to limited in-person consultations and inaccessibility to the healthcare providers nearby, meant that physical examinations and thyroid biopsies may have been hindered during this time.18

The idea of ‘fear of the unknown’ emerged from the interviews, with many patients expressing concerns about not knowing when their treatment would recommence. Not only did the pandemic impact public health services at an operational level but patients also expressed unease towards being treated—whether diagnostic tests or surgery—in a public setting during this time. Consequently, these factors may have elevated patients’ concerns regarding self-perceived risk of disease progression which has also been observed in other cancer types during the pandemic.19 In a recent study of thyroid clinicians’ views towards delayed treatment during the COVID-19 pandemic, most clinicians suggested that while they often did not have concerns regarding disease progression, they worried about the anxiousness patients may face during their delays.4 In other words, clinicians were more worried about the patient’s perception and anxiousness than the actual disease progression.

Active surveillance is a type of management for low-risk thyroid cancers that are now emerging in countries outside Japan; however, this management strategy has differing levels of uptake due to the clinician and patient preferences.20–24 While patients in this study did not undergo active surveillance, it is of interest to consider if a similar management strategy could be used for patients undergoing delays in treatment with regular and planned clinical review. The findings of this study may suggest that discussing the perceived risk of disease and feasibility of active surveillance to eligible patients could alleviate unnecessary concerns surrounding not receiving immediate surgical treatment. However, it is important to note that many of the patients in this study would not have been eligible for active surveillance due to the nature of their tumour sizes and types.

A similar study using semi-structured interviews was conducted in North America, involving patients with breast and prostate cancer. The findings of this study highlighted the importance of ongoing communication between clinicians and patients, as well as patients experiencing anxiousness associated with delays—similar to the findings of this study.8

To our knowledge, this is the first qualitative study to explore the impact of delayed diagnosis and treatment on patients with thyroid cancer during the COVID-19 pandemic. It was important to keep the scope of enquiry broad so as not to restrict the contents of the interviews. The semi-structured nature of the interviews allowed the patients to discuss additional ideas and subthemes for researchers to analyse—niche findings that may not have been captured in a more structured interview format. Additionally, the interview schedule was developed by a multidisciplinary team, which ensured that relevant information was captured.

However, the study is limited by the retrospective nature of the interviews, which may lead to recall bias; interviewing patients during or immediately after their delayed experience may have provided a more robust account of their experience. However, registry-based recruitment was significantly impacted by the COVID-19 pandemic, including the limited capacity to invite participants to studies such as this. Another limitation of this study was that the identification of participants through their treating clinician may have introduced unintended sampling bias to the study. However, the initial stages of this study occurred during the height of the COVID-19 pandemic, and recruitment via the key endocrine surgeons was the most appropriate means of recruitment. While the project also recruited participants via the Australia and New Zealand Thyroid Cancer Registry, the pandemic significantly impacted the core registry operations, including mailing out invitations to potential study participants. The sample was not truly reflective of the population, as this was only a state-based subset of the Australian-based population, and patients from other countries with differing COVID-19 restrictions and healthcare systems may have had different experiences. However, this study was undertaken in Australia when the pandemic was relatively well-controlled, and healthcare restrictions were in place that offered a different insight into the experience of treatment delay. Additionally, non-English-speaking participants were excluded—potentially impacting the generalisability of these findings to a broader population.25 The differences in the length and circumstances surrounding delays varied between patients, which is expected given the variability in restrictions across Australia during this time period, as well as the underlying themes and subthemes we reported. One of the issues faced in this study is potential missing data (i.e., who communicated the treatment delay; method of communication). In future research, it may be beneficial to conduct a supporting quantitative survey to maximise the data completeness, as well as adding the appropriate psychological measures by using validated scales for outcomes like anxiety. It would be of interest to also interview patients who have not experienced delays in their treatment during unexpected delays (i.e., a pandemic), which may allow for comparisons to be made between patients who experience delays versus those who do not.

The COVID-19 pandemic has sharpened the focus on the importance of healthcare communication. During times of unexpected delays, it is vital for clinicians to communicate the perceived risk of disease to patients with thyroid cancer. Providing patients with more accessible information surrounding disease management may ease some of the anxiousness experienced by patients. Additionally, the feasibility of active surveillance should be regularly discussed with patients with low-risk thyroid cancer. Research now suggests that patients can be more accepting of active surveillance when given informed and balanced options for treatment,20 21 26 particularly when clinicians promote this option.20 21 It is also important for clinicians to encourage patients to express their concerns if they are unclear about the information provided to them. Finally, it is imperative that delays are followed up by a medical review to improve overall communication and understanding.