Clinicians' Views on Management and Terminology for Papillary Thyroid Microcarcinoma: A Qualitative Study

Abstract

Background:

There is growing acceptance that the increase in thyroid cancer incidence is in part a result of overdiagnosis of small low-risk papillary microcarcinomas (PMCs) with indolent clinical course. Although surgery is the cornerstone treatment for patients with PMCs, recent management guidelines are shifting toward inclusion of more conservative treatments such as active surveillance. There is little evidence on clinicians' experience in managing PMC patients and their attitudes toward treatment options, including their willingness to accept a nonsurgical option. The aim of this study was to understand how clinicians perceive a diagnosis of PMC, potential changes to terminology, and the treatment options available to patients.

Methods:

This was a qualitative study using semi-structured interviews conducted between November 2015 and May 2016 with 22 clinicians (seven endocrinologists and 15 thyroid surgeons). Transcribed audio-recordings were thematically coded, and a framework method was used to analyze the data.

Results:

Across a sample of clinicians who manage thyroid cancer patients, awareness of overdiagnosis and overtreatment of PMC was common. However, there was little acceptance of active surveillance to manage these patients. Clinicians did not feel comfortable recommending this management approach, as they were worried about the risk of metastases, did not feel that evidence to support this approach was strong enough, and also believed that patients currently have a high preference for surgery. The majority of clinicians did not believe that changing the terminology of this diagnosis was a viable strategy to reduce patients' anxiety and their perceived preference for more aggressive treatments. However, most clinicians felt that thyroid nodules <1 cm should not be biopsied, which could help minimize the risk of overdiagnosis of PMC.

Conclusions:

This study, based on a non-representative sample of 22 clinicians, which remains an important limitation, provides revealing insight into clinicians' management preferences and decision making for small low-risk thyroid cancers at a time when management guidelines and practices are evolving. It suggests that clinicians may not be ready to accept nonsurgical options, or changes in terminology, until evidence to support these options and changes is stronger.

Introduction

Over the last three decades, the incidence of thyroid cancer has risen dramatically worldwide (1), tripling in the United States (2) and Australia (3), and rising more than 15-fold in South Korea (4). The overwhelming majority of these additional cases are papillary thyroid cancers, and approximately half of these are intrathyroidal tumors that are <1 cm (5 –7). As autopsy studies have demonstrated, these papillary microcarcinomas (PMCs) may occur in >10% of subjects, and many remain undetected (8,9). The widespread use of high-resolution ultrasound (US) and US-guided fine-needle aspiration of thyroid nodules, as well as advanced imaging modalities (e.g., computer tomography) has likely increased the detection of PMCs from this large reservoir, and this raises concerns about overdiagnosis (10,11)—the diagnosis of cancers that would not cause harm if left undetected or untreated (12).

Patients diagnosed with PMCs and treated with surgery have a 99% cancer-specific survival rate at 20 years (13). While surgery is an effective treatment modality, it can also result in morbidity (e.g., temporary or permanent laryngeal nerve injury causing damage to the voice), which frequency is directly correlated with the extent of surgical intervention and inversely correlated to the surgeon's experience (14 –16). In addition, following a total thyroidectomy, all patients are required to take lifelong thyroid hormone replacement medication, with approximately one-third of those who have a hemi-thyroidectomy requiring it (17,18). In two studies including 1557 patients, active surveillance of PMCs over a mean follow-up period of 5–6.5 years was associated with no distant metastases or PMC-related deaths, with only about 5% of patients having tumor enlargement ≥3 mm (19 –22). Given the indolence of PMCs, the new 2015 American Thyroid Association (ATA) guidelines note that while surgery is generally recommended for biopsy-proven thyroid cancer, an active surveillance management approach “can be considered” as an alternative to immediate surgery in patients with very low-risk tumors (23). This recommendation presents a challenge to clinicians because the guidelines do not offer comprehensive details about what active surveillance entails (e.g., communication of options or how follow-up is performed). This uncertainty may impact decisions regarding the best treatment choice for individual patients.

Furthermore, besides offering active surveillance, some experts have suggested that changing the nomenclature used for incidentally detected PMCs to convey their indolence more appropriately may make it easier for patients to choose less aggressive intervention for these tumors (10,24,25). These thyroid-specific suggestions are in line with broader calls to change the terminology for a number of indolent lesions with low malignant potential, including, for example, ductal carcinoma in situ of the breast (25,26).

There is currently little research on clinician–patient communication and decision making regarding PMC treatment options, and no research examining the acceptability to clinicians of active surveillance as a management option, or of a change in nomenclature for this condition. This study aimed to understand clinicians' (endocrinologists and thyroid surgeons) experience of managing patients with PMCs, including how a diagnosis is communicated to patients, attitudes toward the various treatment options for patients, and, in particular, their views on active surveillance as a management option and attitudes toward changing the terminology for these tumors.

Methods

Design

This qualitative study used semi-structured telephone interviews to explore clinicians' experience of, and attitudes to, diagnosing and treating patients with PMC.

Sample and recruitment

Participants were 22 medical practitioners involved in the management of thyroid conditions at 13 different medical centers throughout New South Wales, Queensland, and Victoria, Australia.

Medical practitioners were eligible to participate in the study if they were clinicians directly involved in the diagnosis and/or management of PMC patients in Australia. Participants were recruited with the help of collaborators at major endocrine- and cancer-treating hospital networks. All potential participants were given a participant information sheet detailing the aims of and important information about the study. Those interested in taking part returned an expression of interest and consent form to researchers and were contacted to arrange an interview.

Ethical approval was granted by the Sydney Local Health District Ethics Review committee (X15-0155 & HREC/15/RPAH/216) and the QIMR Berghofer Medical Research Institute Human Research Ethics Committee (P1512).

Data collection

The semi-structured interview schedule (Appendix 1) was developed, piloted, and revised by the research team who have expertise across endocrinology (J.B.), public health (B.N. and A.B.), epidemiology (A.B. and S.J.), psychology (K.M.), health communication (B.N. and K.M.), and overdiagnosis (B.N., J.B., A.B., S.J., R.M., and K.M.). The interviews were conducted over the telephone by a researcher with experience in qualitative research methods (B.N.) between November 2015 and May 2016. Interviews lasted approximately 20 minutes, and were audio-recorded and transcribed verbatim. The researcher conducting the interview also made notes during and after the interview regarding any relevant information about the interview, including questions or points to clarify with the practicing endocrinologist and thyroid expert on the study team (J.B.).

Analysis

The study used a phenomenological methodology to understand clinicians' experiences and perspectives, and a thematic analysis of the transcribed interviews was conducted using framework analysis in Microsoft Excel to organize the data to capture the views expressed by participants (27). One researcher (B.N.) reviewed the transcripts and developed a list of emerging topics and themes arising from the transcripts. Those themes, along with the interview schedule, formed the basis of the coding framework. An additional two researchers (J.B. and K.M.) read a subset of transcripts and reviewed the coding framework, and necessary changes or additions to the framework were discussed and made. Once a framework was agreed upon, one researcher (B.N.) coded all of the interviews into the coding framework, which was validated by an additional researcher (K.M.). Prominent themes arising from the coding framework were then identified and discussed in depth with the entire research team.

Results

Participant characteristics are shown in Table 1. The clinicians interviewed included seven endocrinologists and 15 thyroid surgeons, with an average of 16 years of experience. Interviewed clinicians practiced at a range of hospitals and/or clinics including urban and rural centers. The clinicians reported they treated between 2 and 30 new thyroid cancer patients per month, including patients with PMCs diagnosed preoperatively (diagnosed before any surgical intervention).

Table 1.

Clinician Characteristics

Characteristic	Number of clinicians (n = 22)
Specialty
Endocrinologist	7
Surgeon	15
Years of experience
<10	6
10–19	9
20–29	3
30+	4
Type of hospital or practice
Urban	17
Rural	5
Sex
Male	17
Female	5
Approx. amount of new thyroid cancer patients/month
<5	9
5–10	7
10+	6

To illustrate the study findings, key themes emerging from the interviews are described below. Clinicians' quotations have been selected that demonstrate common responses as well as the diversity of the attitudes expressed. A summary of the key themes with supporting quotes are also presented in Table 2.

Table 2.

Summary of Key Themes

Theme	Summary	Supporting quote(s)
Clinicians' views on how PMC are identified	Clinicians reported it was uncommon for them to biopsy patients with thyroid nodules <1 cm, and that increasing use of scans seemed to be the main reason that these small thyroid cancers were being identified	“I think, I mean we're certainly seeing a significant increase in thyroid cancer in my practice so, over the last decade or so. And so, I think that, because of technology and because of the burgeoning of availability out there in the community, there are more and more ultrasounds and you know, a number of patients are being picked up with incidental findings if you like. So not necessarily having it done for their thyroid but seen on an ultrasound or seen on PET scan or seen on something else, taken to that conclusion and they end up having that diagnosis.” (ID13, surgeon, 30 years' experience)
Attitudes toward overdiagnosis and overtreatment of PMC	Clinicians were aware that a diagnosis of PMC may be clinically insignificant in many patients but believed that surgical treatment was necessary	“As it's becoming increasingly clear that thyroid cancer is not a, a disease that people die of, so it's really about managing, … managing the indolent cancers in a way that's not going to cause harm to the patient.” (ID1, surgeon, 6 years' experience) “So, if you like, the ATA guidelines for needle biopsy are designed to avoid over diagnosis … and for avoiding the microcarcinomas flooding our system.” (ID8, endocrinologist 20 years' experience)
Treatment decision-making pathway	Surgeons felt that patients were primed for surgery by the time the surgeons were involved in the treatment decision-making process	“Usually, by the time they've been referred to us, they know they're probably heading for an operation.” (ID12, surgeon, 16 years' experience)
Treatment clinicians offer and prefer	The majority of clinicians only describe offering patients the option of surgery, with a few discussing the option of active surveillance with their patients at this time	“We give them the option as to whether they would just have a hemi-thyroidectomy or a total thyroidectomy. Because the prognosis would be unchanged with either approach.” (ID3, surgeon, 9 years' experience) “In general, we're still recommending some surgery … but we bring up the observation studies that are being performed elsewhere.” (ID7, endocrinologist, 5 years' experience)
Clinicians' views on patients' preference for management	Clinicians held the view that patients would not be reassured about having a cancer if it was not surgically removed	“I would predict that 10 out of 10 times you tell people that they have cancer in their neck, then they will say, well, when is it coming out.” (ID4, endocrinologist, 9 years' experience)
Acceptance of active surveillance	Many clinicians felt that the evidence to support active surveillance was not strong enough; those who were more accepting of active surveillance would only be comfortable with it under certain circumstances or with patients who had specific clinical characteristics	“But at the moment there's not enough evidence to say, in my view, that it's [active surveillance] safe. The only studies that you've got are from Japan as far as I know.” (ID14, surgeon, 24 years' experience) “Yeah, I mean, so if there was nothing else on ultrasound, if there were no other risk factors, so smoking, family history of thyroid cancer, radiation exposure, all the stuff that we know of. So if all that came back fine and, look, if we even have the benefit … I'd be pretty comfortable … to adopt a more conservative approach, so.” (ID9, endocrinologist, 10 years' experience)
Cultural difference in accepting active surveillance	Clinicians were concerned about the applicability of active surveillance studies to non-Japanese populations	“There are a lot of ways these things are managed in Japan that people wouldn't think of managing, even bigger nodules. They do hemis for a lot of things in Japan that we wouldn't do here in Australia or the United States … That's again, mainly because it's, it's a cultural thing even, that patients are just not as prepared to live with a cancer. Whereas in Japan that sort of seems to be … they're a bit more philosophical about it.” (ID11, endocrinologist, 30 years' experience)
Clinicians worry about the risk of progression	Clinicians were worried about their duty of care, as there is currently no way to determine which tumors would progress and metastasize and which would not	“I have concerns about whether tumors do undergo transformation to more high-grade tumors over time. And I don't know that if that is the case that we can select them out well. So I'm concerned about patients with a life expectancy >10 years of suggesting monitoring because, you know, what's relatively simple treatment can turn into a life-threatening situation.” (ID3, surgeon, 9 years' experience)
Attitudes toward changing the terminology	Clinicians did not want to change the terminology due to the risk of progression, which they acknowledge was low	“Oh, I mean, I'd be reluctant to change the term “carcinoma” 'cos we've all had patients where even a small microcarcinomas presented with fairly extensive node metastasis. It's not common, I know they're not common. But … it still happens.” (ID1, surgeon, 6 years' experience)

Clinicians views on how PMCs are identified

Both endocrinologists and surgeons mentioned that it is uncommon for them to biopsy patients with thyroid nodules <1 cm. The general feeling was that most clinicians in Australia had followed this practice for a number of years. Consequently, only a small number of patients were diagnosed preoperatively with PMCs in their practices.

A centimetre is the, is the cutoff that most people use. Some ultrasound guys are getting a bit more aggressive trying to stick needles into really tiny things. (ID11, endocrinologist, 30 years' experience)

Generally, the practice is, in my experience, that if you've got a tiny nodule in your thyroid, we wouldn't biopsy it because it's hard to do. (ID14, surgeon, 24 years' experience)

However, clinicians went on to discuss why patients with nodules <1 cm would sometimes get biopsied and therefore why some PMCs are diagnosed preoperatively. Clinicians reported that increasing use of scans seems to be the main reason that these small thyroid cancers were being identified.

I think, I mean, we're certainly seeing a significant increase in thyroid cancer in my practice so, over the last decade or so. And so, I think that, because of technology and because of the burgeoning of availability out there in the community, there are more and more ultrasounds and, you know, a number of patients are being picked up with incidental findings, if you like. So, not necessarily having it done for their thyroid, but seen on an ultrasound or seen on PET [positron emission tomography] scan or seen on something else, taken to that conclusion and they end up having that diagnosis. (ID13, surgeon, 30 years' experience)

Attitudes toward overdiagnosis and overtreatment of PMC

Awareness of overdiagnosis and overtreatment of thyroid cancer, in particular PMCs, seemed to be common among clinicians. A number of clinicians discussed this in relation to the indolent nature of the diagnosis.

As it's becoming increasingly clear that thyroid cancer is not a … a disease that people die of, so it's really about managing, … managing the indolent cancers in a way that's not going to cause harm to the patient. (ID1, surgeon, 6 years' experience)

But most of the patients, if they know they've got a cancer of the thyroid, want something done about it, then I'm happy to do that for them. But, you know, I realize that we're probably overtreating them. (ID13, surgeon, 30 years' experience)

One in four people, they die with thyroid cancer, not necessarily of thyroid cancer… (ID18, surgeon, 16 years' experience)

A few clinicians also discussed overdiagnosis in relation to the new ATA guidelines. They understood that these guidelines were updated to help reduce the number of PMC cases being identified.

So, if you like, the ATA guidelines for needle biopsy are designed to avoid overdiagnosis … and for avoiding the microcarcinomas flooding our system. (ID8, endocrinologist, 20 years' experience)

Although clinicians were aware that a diagnosis of PMC may be clinically insignificant in many patients (as expressed in the quotations above), they still believed that surgical treatment was necessary. Most clinicians interviewed considered surgery (hemi-thyroidectomy or total thyroidectomy) as the only option to manage patients diagnosed with PMC.

I'll talk about just taking out half of the thyroid and leaving the other half because it's less, less risk to the patient and less chance that they're going to need to be on thyroid hormone replacement therapy. And it's a highly curable cancer so you know it's, it's a very good option for them. (ID1, surgeon, 6 years' experience)

Hemi-thyroidectomy. That would be the smallest operation I'd do. (ID16, surgeon, 24 years' experience)

Treatment decision making

Treatment decision-making pathway

The treatment decision-making process for PMC can involve a number of clinicians, including general practitioners (GPs), endocrinologists, and surgeons. The various clinicians involved and the pathways leading to treatment were issues emerging in the interviews with the surgeons when they discussed how they manage patients based on how the patients present to them.

I'll be referred patients directly from GPs or from endocrinologists. Depending who the referral is from, if it's from an endocrinologist, it's usually with the diagnosis. If it's from a GP, it's usually a thyroid nodule. And if it's a thyroid nodule, then we'll arrange the needle biopsy, do the surgery, and manage them postoperatively as well. (ID3, surgeon, 9 years' experience)

Overall, surgeons felt that patients were primed for surgery by the time the surgeons were involved in the treatment decision-making process.

Usually, by the time they've been referred to us, they know they're probably heading for an operation. (ID12, surgeon, 16 years' experience)

Yeah, well, they've usually been told that they've got a papillary thyroid cancer. They usually want something done about it when they come in the door. (ID13, surgeon, 30 years' experience)

Treatments clinicians offer and prefer

Both endocrinologists and surgeons discussed the treatments they offer to patients, with the majority only describing offering patients the option of surgery, including hemi-thyroidectomy or thyroidectomy. However, there were a few endocrinologists and surgeons who discussed that they had recent conversations with patients about the option of active surveillance. Although this option was discussed with patients, these clinicians did not seem to recommend this management approach or necessarily feel comfortable with it.

Generally speaking, I would say, well, we'll do your total thyroidectomy, although these days of course the guidelines have changes with the Australian, er, the ATA guidelines have just recently changed, and so it's felt that for micro cancers that hemi-thyroidectomies is probably enough. (ID14, surgeon, 24 years' experience)

We give them the option as to whether they would just have a hemi-thyroidectomy or a total thyroidectomy. Because the prognosis would be unchanged with either approach. (ID3, surgeon, 9 years' experience)

In general, we're still recommending some surgery … but we bring up the observation studies that are being performed elsewhere. (ID7, endocrinologist, 5 years' experience)

Clinicians' views on patients' preferences for management

Clinicians discussed their views on what they believed patients preferences were for treatment. Many clinicians seemed to justify their preference for surgery by what they believed was what patients would want.

I would still probably remove it. Because I think in the current sort of climate, most people would want it removed. (ID4, endocrinologist, 9 years' experience)

Many clinicians also believed that this patient preference for surgery was a result of them being diagnosed or hearing the term “cancer.” They believed that patients would not be reassured about having a cancer if it was not taken out surgically.

I think the other thing to consider is the fact that there are plenty of patients where if you tell them that they have a cancer in their thyroid, and you'd like to keep an eye on it and sort of reassure them that it's ok … they're not going to be adequately reassured by that. (ID5, surgeon, 2 years' experience)

I would predict that 10 out of 10 times you tell people that they have, cancer in their neck, then they will say, well, when is it coming out. (ID4, endocrinologist, 9 years' experience)

Clinicians perceived that patients generally had difficulty with treatment decision making and had a high reliance on their clinicians to help them make a decision about treatment. The majority of clinicians said they felt that they ultimately have the final decision in what treatment the patient receives.

I think there are a few people who will go home and think about it, but the vast majority of people just say, look, just do whatever you think, and, and leave it up to us to make the decision for them. (ID1, surgeon, 6 years' experience)

But the reality is that at least in the environment where I practice, I find that there are many people that find it very difficult to make the decision once you give them all the pros and cons of each approach, and they want to leave it in my hands. (ID5, surgeon, 2 years' experience)

Most often, I make the recommendation. It's too hard for patients to navigate through written material and arrive at their own decision. (ID8, endocrinologist, 20 years' experience)

Attitudes toward active surveillance as a management option

Overall acceptance of active surveillance, including feelings toward evidence of active surveillance

Acceptance of active surveillance among the clinicians interviewed varied. Among the sample of clinicians, about half of both endocrinologists and surgeons discussed being accepting of this option—but didn't necessarily offer it. Equally, about half of endocrinologists and surgeons were opposed to it. There were no major differences between endocrinologists and surgeons on acceptance of surveillance among this sample. Four clinicians (one endocrinologist and three surgeons) discussed having experience of offering the option of active surveillance to their patients, with two of them having experience of a patient taking up and following an active surveillance management approach. The clinicians (both endocrinologists and surgeons) who seemed more accepting of this approach stated that they would only be comfortable with it under certain circumstances such as the patient not wanting surgical interventions or with patients who had specific clinical characteristics.

Yeah, I mean, so if there was nothing else on ultrasound, if there were no other risk factors, so smoking, family history of thyroid cancer, radiation exposure, all the stuff that we know of. So if all that came back fine and, look, if we even have the benefit … I'd be pretty comfortable … ah, to adopt a more conservative approach, so. (ID9, endocrinologist, 10 years' experience)

If I'm going to offer the watchful waiting, I need to be happy in my own mind that the patient will tick those boxes [favourable location of the lesion and patient commitment to follow-up]. (ID19, surgeon, 16 years' experience)

Although a number of clinicians indicated that they could be accepting of active surveillance in specific circumstances (e.g., if the patient preferred this option or had a shorter life expectancy), overall clinicians felt that there was not enough evidence to support the safety of active surveillance.

But at the moment, there's not enough evidence to say, in my view, that it's [active surveillance] safe. The only studies that you've got are from Japan as far as I know. (ID14, surgeon, 24 years' experience)

I think that the data are not really strong in that [active surveillance]. (ID3, surgeon, 9 years' experience)

Cultural differences in accepting active surveillance

Some clinicians believed that active surveillance was culturally rooted and that patients in Australia would not be as comfortable with that approach as patients in Japan where the studies on active surveillance have been conducted.

There are a lot of ways these things are managed in Japan that people wouldn't think of managing, even bigger nodules. They do hemis for a lot of things in Japan that we wouldn't do here in Australia or the United States … That's again mainly because it's, it's a cultural thing even, that patients are just not as prepared to live with a cancer. Whereas in Japan that sort of seems to be … they're a bit more philosophical about it. (ID11, endocrinologist, 30 years' experience)

Clinicians worry about the risk of progression

Acceptance of active surveillance was also limited by clinicians attitudes about the risk of the papillary thyroid cancer progressing. Overall, clinicians were worried that if they did take an active surveillance management approach, then the tumor might metastasize. It was apparent that they were worried about their duty of care as clinicians, as there is currently nothing to determine which tumors would progress and which would not.

I have concerns about whether tumors do undergo transformation to more high-grade tumors over time. And I don't know that if that is the case that we can select them out well. So I'm concerned about patients with a life expectancy >10 years of suggesting monitoring because, you know, what's relatively simple treatment can turn into a life-threatening situation. (ID3, surgeon, 9 years' experience)

I think we need better tests to discriminate who is going to be a problem … with subsequent nodal metastases. (ID8, endocrinologist, 20 years' experience)

It's, it's, it's a medicolegal problem to say to somebody, “You don't need any further treatment”, and then for them to come back 5 or 10 years later with a nodal recurrence and for them to then ask, “Well, why wasn't I treated properly the first time? Why did you let this metastasize?” (ID8, endocrinologist, 20 years' experience)

Attitudes toward changing the terminology

Overall, clinicians were opposed to the idea of changing the terminology for small papillary thyroid cancers. Concern about the risk of progression of PMCs, which they acknowledged was low, was the main reason why clinicians did not want to change the term.

Oh, I mean, I'd be reluctant to change the term “carcinoma” 'cos we've all had patients where even a small microcarcinomas presented with fairly extensive node metastasis. It's not common, I know they're not common. But … it still happens. (ID1, surgeon, 6 years' experience)

You do have that small proportion of people who have microcarcinomas that do metastasize … or do progress and we can't predict those at the moment. (ID7, endocrinologist, 5 years' experience)

In contrast, clinicians acknowledged that the term “cancer” does make both patients and clinicians more anxious and inclined to have surgery.

I know even among the medical profession, the word “cancer” does invoke a fairly stringent response. (ID13, surgeon, 30 years' experience)

Well, I must say, in my experience, there are very few patients in my practice who would be happy to know that they've got a cancer in them and we're going to watch it. (ID14, surgeon, 24 years' experience)

Some clinicians believed that discussing the low risk of the condition with the patient, rather than changing the terminology, would be a more adequate strategy to decrease patient anxiety and potentially reduce preference for more aggressive treatment options.

I think the key really is that you need to spend enough time with your patient to explain the differences in progression and the outlook. (ID2, endocrinologist, 15 years' experience)

I would rather, yes, give patients complete and accurate information, and say, you've got this kind of cancer but, you know, according to these criteria, it's very low risk and therefore, you know, your risk of whatever is this percent. (ID4, endocrinologist, 9 years' experience)

Discussion

Principal findings

The findings from this qualitative interview study of Australian endocrinologists and thyroid surgeons suggest that although there is awareness of overdiagnosis and overtreatment of low-risk papillary thyroid cancers, clinicians are generally not yet comfortable recommending active surveillance as a management approach for a diagnosis of PMC. Their main concerns with this management approach were the risk of progression of the lesion and the feeling that evidence to support the safety of this approach was insufficient, although it has been reported that the incidence of unfavorable events is lower in patients who choose active surveillance (4,28). Clinicians did not feel comfortable knowing that a small number of patients diagnosed with PMCs could develop metastases, and that there was no way of currently knowing which patients they might be. Clinicians also believed that at this time, patients preferred a surgical management approach, as they tend to be anxious when diagnosed with cancer, and active surveillance would not provide them with adequate reassurance.

These concerns underscore an important issue surrounding the evidence to support an active surveillance management approach and current practice. Evidence from observational studies show that the rate of locoregional metastases with active surveillance is comparable to the rate that can occur after thyroid surgery, and that outcomes of surgery for PMC are the same irrespective of whether surgery is undertaken immediately or after any progression (19 –21,28,29). Furthermore, patients who develop local recurrence after surgery will still require a second surgery, and having only one surgery after progression may be better for patients, since their final outcomes are similarly excellent (30).

Overall, clinicians in this study reported thinking the evidence to recommend active surveillance routinely is not strong enough, and did not cite a need for randomized trial evidence before changing their practice. Rather, the uncertainty of the evidence seems to arise from concerns about the applicability of the evidence beyond non-Japanese populations. An ongoing cohort in the United States, however, has reported similar findings in a predominantly white Caucasian population (31). Other possible explanations for the preference of clinicians for surgery over active surveillance include that the guidelines supporting active surveillance in patients with PMC have only been published relatively recently; the way in which the recommendation is framed (“can be considered”); or because the guidelines do not discuss the wide variety of clinical factors that need to be taken into account when considering active surveillance.

It is important to note that the majority of clinicians in this study agreed that thyroid nodules <1 cm do not require a biopsy. As suggested by this study and current trends in the United States (32), clinical practice to biopsy nodules <1 cm is decreasing. If this practice becomes more widespread, PMCs will not be diagnosed. However, it is still unclear whether this shift in practice will affect the number of patients enrolled in active surveillance protocols. A highly suspicious 0.8 cm thyroid nodule (risk of malignancy 70–90%) may not require a biopsy according to new guideline recommendations, but it may require follow-up that resembles an active surveillance protocol for PMC (yearly neck USs). This is particularly relevant for younger patients in whom the risk of growth and metastasis is higher than in elderly individuals (5% vs. 2% in 10 years) (19,20). Active surveillance for suspicious small nodules may indeed be more accepted by clinicians that are accepting of active surveillance for biopsy-proven thyroid cancers. This is supported by the responses of the interviewed clinicians that strongly encouraged efforts to reduce overdiagnosis by reducing the number of biopsies, yet still recommend surgery once cancer is cytologically diagnosed. This implies that the driver to treat a biopsy-proven PMC is not really the underlying biology of the disease, but rather the knowledge of cancer and the perceived need that something has to be done.

Finally, clinicians did not favor changing the name of this condition to remove the term “carcinoma,” even though this may be a strategy to reduce anxiety and potentially enable patients to feel more comfortable with choosing less aggressive treatment options. For other indolent tumor types (e.g., ductal carcinoma in situ of the breast), this strategy has been shown to increase preference for more conservative treatments, including active surveillance, at least in hypothetical scenarios (33,34). In addition, a recent change in the terminology of the noninvasive encapsulated follicular variant of papillary thyroid carcinoma to exclude the term “carcinoma” has also been implemented, as it was shown that it rarely exhibits lymph node metastases and behaved indolently, similar to follicular adenomas (35,36). This research and small practice change emphasizes that simply changing the terminology used to describe indolent tumors such as PMC may be an effective strategy for mitigating overdiagnosis and overtreatment (37).

Strengths and limitations

To the authors' knowledge, this is the first study to explore clinicians' views on overdiagnosis and overtreatment of low-risk cancers. Specifically, this study provides insight into factors that influence treatment preferences and decision making of clinicians managing patients with PMCs. Although a few studies have looked at community views on overdiagnosis more generally and across other conditions (38 –41), clinicians' views are not well understood. Furthermore, qualitative views specifically on the management of small thyroid cancers, and potential changes to terminology, have not been explored.

Interviewing both endocrinologists and surgeons is another strength of the study, as the diagnostic pathway of PMC is complex, and both types of clinicians are usually involved. The clinicians in this study also varied widely in their experience and in the type of center in which they generally practiced.

This study has, however, several limitations. Interviews were only conducted with clinicians (endocrinologists and thyroid surgeons) specifically involved in thyroid cancer management and who agreed to take part; other clinicians (GPs or radiologists) who may also be involved were not interviewed. Furthermore, a sample of only 22 Australian clinicians were interviewed in this study, although this sample size is common in qualitative research, which seeks to portray depth and detail rather than statistical representativeness. All data presented are qualitative and therefore axiomatically based on researchers' analysis and interpretation of clinician comments and reported experiences. As such, views and attitudes about the risk of overdiagnosis of PMC and attitudes toward active surveillance may not be generalizable and may differ from clinicians in other countries. The treatment preferences, attitudes to changing the terminology, and experiences of patients with PMCs were also not included in this study. However, this sample is being studied currently by the research team, and results will be reported separately.

A further limitation is that much of the data were coded by one researcher, and may be prone to investigator bias. However, several members of the author team, including a thyroid expert clinician, were involved in reading transcripts; formulating, reviewing, and testing the coding framework; and the analysis, as is common in qualitative research.

Impact on research and practice

This study demonstrates that clinicians managing PMC patients may need more guidance and evidence on how better to select patients for and manage patients with active surveillance. Although interventions to support this are not yet widespread, a recent clinical framework to facilitate risk stratification when considering this approach has been developed (42). This framework may help improve the ability of clinicians, such as those in this study, to identify and feel comfortable suggesting or recommending active surveillance to patients who may benefit. Furthermore, an educational module from the Thyroid Cancer Care Collaborative (TCCC) guides clinicians on how to choose ideal patients for active surveillance and how to help them follow these patients. This module is part of a larger online tool developed by the TCCC to help active surveillance protocols be successfully implemented outside Japan (43,44).

The present findings also suggest that clinicians working with thyroid cancer may need to give a higher priority to shared decision making (SDM) surrounding treatment decisions with patients, including now discussing and offering them the option of active surveillance. Educating clinicians as well as patients and the general public on the option of active surveillance is important, as patients need to be aware of all of their treatment options so that they can make an informed choice that best aligns with their values and preferences. Although many efforts and a certain length of time is needed, without sufficient knowledge and confidence, clinicians cannot give adequate information to their patients. Decision aids may be one tool that clinicians can use to help facilitate SDM (45), and a group at the Mayo Clinic is currently testing how a decision aid for patients with small papillary thyroid cancer may help clinicians and patients achieve better SDM (NCT02878044).

Conclusion

In light of recent guidelines that state “an active surveillance management approach can be considered as an alternative to immediate surgery in patients with very low-risk tumors” (23), as well as the emerging evidence of overdiagnosis and overtreatment of PMCs and the safety of active surveillance (19,21,29), this study provides important insight into clinicians' treatment preferences and decision making for these small low-risk thyroid cancers at a time when management guidelines and practices are evolving. It demonstrates that overall, clinicians managing these patients may not be ready to accept nonsurgical management approaches, or a change in terminology, until evidence or guidelines are stronger. Support and training interventions for clinicians about how to offer active surveillance safely may also need to be more readily available and endorsed by relevant specialist authorities.

Footnotes

Acknowledgments

We would like to thank the clinicians who participated. B.N. was supported by the Sydney Catalyst Research Scholar Award. A.B., R.M., and K.M. are investigators on a National Health and Medical Research Council of Australia (NHMRC) funded CRE grant No.1104136. S.J. and K.M. are supported by fellowships from the NHMRC. The funders had no role in the design or conduct of the study; in the collection, analysis, and interpretation of the data; or in the preparation or approval of the manuscript.

Author Disclosure Statement

A.B. and R.M. were co-chairs of the steering committee for the 2016 Preventing Overdiagnosis international scientific conference. All other authors declare that they have no competing interests.

Appendix 1. Clinician Interview Schedule

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