Endocrinologist-Perceived Factors Affecting the Transition of Thyroid Cancer Patients from Specialist to Primary Care Postcancer Treatment in Ontario,Canada

Abstract

Background:

Methods:

All eligible practicing endocrinologists in Ontario were invited to participate in the study, via an email with an embedded survey link. Consent was assumed if the physician completed the survey. The survey collected physician demographics and asked a series of Likert-scale and open-ended questions on their views regarding transitioning care of their thyroid cancer patients. Quantitative analysis was based on mode and variability. Qualitative analysis was completed using inductive thematic analysis.

Results:

Seventy physicians completed the survey, with a response rate of 35.5%. Based on the responses to the Likert-scale questions, there was a lack of consensus in terms of discharging criteria for patients who had low-risk papillary thyroid cancer, stable thyrotropin levels, multiple nonthyroid-related comorbidities, and hemithyroidectomy with no disease recurrence. The majority of endocrinologists responded that the main factors affecting discharge included whether the primary care physician was able to follow their recommendations, whether the primary care physician could appropriately adjust levothyroxine doses, and whether the patient was confident that their primary care physician could manage their thyroid cancer follow-up. Themes extracted from the open-ended question also indicated that the main factors affecting the transition of care were related to the primary care physician, the patient, the imaging interpretation, and the discharge guidelines.

Conclusion:

The lack of consensus among endocrinologists affects the transition of patient care, and there is a need to provide clear and accurate information to primary care physicians and thyroid cancer patients on postcancer treatment care. Efforts should be sought to standardize discharge and long-term care.

Background

Of all types of cancers, thyroid cancer is increasing the most rapidly in Canada (1). An estimated 8200 Canadians are diagnosed each year (2) and it is now the fifth-most common cancer in Canadian women (3). Despite this, the 5-year survival rate is over 97% (1). Over 80% of thyroid cancer patients present with well-differentiated thyroid cancers (4), which includes papillary and follicular tumors. After initial surgery and adjuvant treatment, these patients are often followed indefinitely by an endocrinologist who monitors for cancer recurrence through periodic blood tests and neck ultrasounds. However, with the rising incidence of thyroid cancer, the need for long-term follow-up, and the limited number of thyroid cancer specialists and primary care physicians are ideally positioned to play an important role in post-treatment thyroid cancer care.

Much of what is known about cancer survivorship and transitioning care from specialist to primary care physician comes from the breast and colorectal cancer survivorship literature (5,6), where the role of the primary care physician is well established. Previous studies in these cancers have shown that exclusive primary care physician follow-up is not associated with delay in diagnosing recurrence or an increased rate of serious clinical events (7,8). Furthermore, breast cancer survivors' quality-of-life scores actually increased when primary care physicians assumed greater responsibility for ongoing care (9,10). Thus, primary care physicians can play an important role in the long-term follow-up of cancer survivors, including screening for recurrence, managing comorbid conditions, as well as health promotion. However, the role of primary care physicians in long-term thyroid cancer care to date has been limited. Previous literature on thyroid cancer survivors has shown that possible patient barriers include side effects from thyroid hormone fluctuation, fear of disease recurrence, and lack of confidence in the ability of the primary care doctor to manage thyroid cancer follow-up (11 –15).

Thyroid cancer patient discharge patterns from specialists are heterogeneous, with some specialists following patients for a longer period of time than others. With no well-established transitional plan, unlike in breast and colorectal cancer, primary care physicians play a variable role in contributing to long-term thyroid cancer care. Although Cancer Care Ontario has recently published clinical pathways for thyroid cancer treatment, which include guidance for transition to a primary care physician within one to five years from diagnosis for low-risk patients (16), the facilitators and barriers affecting this transition have not yet been examined. Thus, the objective of this study was to examine endocrinologist-perceived factors affecting the transition of care for thyroid cancer patients through a qualitative and quantitative survey of active endocrinologists in the Canadian province of Ontario.

Methods

Participants

Eligible endocrinologists included all practicing endocrinologists identified through the College of Physicians and Surgeons of Ontario and the Ontario Medical Association (OMA). In Ontario, membership in the OMA is mandatory for physicians and consequently, we are confident that invitations were sent to all eligible endocrinologists. We did not invite pediatric endocrinologists to participate since they do not discharge their patients to primary care. REB approval was obtained for this study.

Endocrinologists were deemed ineligible if they were (i) retired, (ii) practiced outside Ontario, or (iii) did not treat adult patients with thyroid cancer (which was declared by an endocrinologist at the time of recruitment).

Recruitment

Endocrinologists were recruited between March and April 2019. All practicing endocrinologists eligible for the study in Ontario were sent an email from the principal investigator, inviting them to participate in the study, via an embedded SurveyMonkey link. Emails were acquired from hospital or academic institution websites based on physician affiliations. One reminder email was sent two weeks after the initial email. A paragraph at the beginning of the survey described the purpose of the study and consent was assumed if the physician completed the survey. Study participation was solely voluntary, with no remuneration provided.

Survey

The survey included a section on demographics, where information on sex, years in practice, population size in the location of practice, and approximate percentage of thyroid cancer patients in their practice was collected.

A Likert-scale questionnaire was designed through collaboration with thyroid cancer specialists at the University of Toronto and statisticians and experts in qualitative research methodology and knowledge translation at the University of Toronto's Wilson Centre. The development of the questionnaire for the current study involved adapting questions used in previously published research on transition of care in breast and colon cancer, including emulating focus group questions and survey topics (5 –9,17).

The Likert-scale questionnaire was used to assess endocrinologists' views. The first section consisted of 12 items to assess in what specific scenarios patients would be discharged to their primary care physician (1 = never discharge, 3 = discharge 50% of the time, and 5 = always discharge).

The second section consisted of 8 items designed to assess perceived endocrinologist factors to discharging patients back to their primary care physician (1 = not important, 3 = neutral, and 5 = very important). Lastly, the survey had an open-ended question for endocrinologists to describe any significant factors to transitioning the care of patients with papillary thyroid cancer to their primary care physician.

Quantitative analysis

Data were analyzed using the Statistical Package for Social Sciences (SPSS, Chicago, IL). Descriptive statistics were used to describe the study population.

Many responses to the Likert-scale questionnaire did not follow a bell curve distribution, thus using the mean response for each question would not accurately represent the majority's response. Thus, each Likert-scale question was assessed using the mode and the variability of responses was assessed by population skewness, where 0 = a bell curve distribution, thus a wide range of answers. The more positive the number, the more the long tail of the graph fell to the right and more participants chose a Likert response closer to 1. The more negative the number, the more the long tail of the graph fell to the left of the graph and more participants chose a Likert response closer to 5.

For the first set of questions regarding how likely would it be that participants would discharge certain patient populations to primary care physicians, skewness was defined as 0 = a bell curve distribution, whereas the more positive the number, the greater distribution of answers toward never discharge, and the more negative the number, the greater distribution of answers toward always discharge. For the second set of questions regarding how important certain factors were for discharge, skewness was defined as 0 = a bell curve distribution, whereas the more positive the number, the greater the distribution of answers toward not important, and the more negative the number, the greater the distribution of answers toward very important.

Qualitative analysis

The qualitative responses were coded by two independent members of the research team on NVivo 10 software using inductive thematic analysis (18). The codes were compared and discussed to achieve triangulation of the data and coding ceased when saturation was achieved (19). The codes were then sorted into groups to achieve themes and subthemes based on their relationship with one another (20).

Ethical considerations

Ethics approval for the study was provided by the University of Toronto Research Ethics Committee, Toronto, Canada.

Results

Of 197 possible participants, 70 completed the survey, with a response rate of 35.5%.

Participant characteristics

Of the respondents, 50.7% were female, 44.9% were male, and 4.3% preferred not to disclose. The number of years of practice ranged from <5 (30.8%), 6 to 10 (16.2%), 11 to 25 (33.8%), and >25 (19.1%). The majority of respondents practiced in a location with a population size >1 million (61.6%) and reported that the percentage of patients with papillary thyroid cancer in their practice ranged from 6% to 25% (Table 1).

Table 1.

Physician Demographics

Characteristic	Count (%)
Sex (n = 68)
Female	35 (50.7%)
Male	31 (44.9%)
Prefer not to answer	3 (4.3%)
Years in practice (n = 68)
<5	21 (30.8%)
6–10	11 (16.2%)
11–25	23 (33.8%)
>25	13 (19.1%)
Population of city of practice (n = 60)
<500,000	13 (21.6%)
500,000–1 million	10 (16.6%)
>1 million	37 (61.6%)
% of papillary thyroid cancer patients in practice (n = 70)
<5	15 (21.5%)
6–25	46 (65.5%)
25–50	8 (11.5%)
>50	1 (1.5%)

Quantitative responses

Patient populations to discharge

As shown in Table 2, responses were more dispersed in terms of discharging patients with low-risk papillary thyroid cancer (mode = 3, skew = +0.11), stable thyrotropin (TSH) but experiencing fatigue (mode = 3, skew = −0.08), multiple nonthyroid-related comorbidities (mode = 2, skew = +0.08), and hemithyroidectomy with no disease recurrence (mode = 2, skew = +0.19). However, there was consensus regarding not discharging patients who were high risk (skew = +1.67), or who had nonspecific cervical lymphadenopathy (skew = +1.67), recurrence of neck disease that was stable (skew = +3.38), and stable lung nodules (skew = +6.61).

Table 2.

Quantitative Histogram Distribution of How Likely Are Endocrinologists to Discharge Specific Patient Populations Back to Primary Care Physician (n = 70)

Patient population^a	Mode (1 = never discharge, 5 = always discharge)	Population skewness (0 = bell curve distribution, + = long tail on right, − = long tail on left)
ATA-defined low-risk thyroid cancer patient	3	+0.11
ATA-defined moderate-risk thyroid cancer patient	1	+0.92
ATA-defined high-risk disease (even though no evidence of recurrence)	1	+1.67
Enlarged cervical lymph nodes or small lesions in the thyroid bed (even if they are nonspecific and are not growing)	1	+1.67
Proven disease in the neck (even though not progressing)	1	+3.38
Persistent disease in lungs (even though not progressing)	1	+6.61
Persistent symptoms of fatigue (even though TSH at target)	3	−0.08
Fluctuating TSH necessitating frequent dose adjustments of thyroid hormone replacement	1	+0.91
Multiple comorbidities (unrelated to thyroid cancer)	2	+0.08
Women with future pregnancy plans in the next five years	1	+0.69
Hemithyroidectomy only (even though no recurrence in contralateral lobe)	2	+0.19
Hypoparathyroidism as a result of thyroid cancer surgery	1	+0.72

The patient populations were presented in a 12-scenario question on the participant study questionnaire, inquiring on the likelihood of discharging patients back to primary care physicians.

ATA, American Thyroid Association; TSH, thyrotropin.

Factors affecting decision to discharge

As shown in Table 3, the majority of endocrinologists responded that the main factors affecting their decision to discharge included whether the primary care physician was able to follow their recommendations (skew = −1.77), confidence in the primary care physician's ability to appropriately adjust levothyroxine doses (skew = −1.19), and the patient's perception that their primary care physician could manage their thyroid cancer follow-up (skew = −1.10).

Table 3.

Quantitative Histogram Distribution of Endocrinologist-Perceived Factors to Discharging Papillary Thyroid Cancer Patients Back to Primary Care Physician (n = 70)

Perceived factor^a	Mode (1 = not important, 5 = very important)	Population skewness (0 = bell curve distribution, + = long tail on right, − = long tail on left)
You are easily able to communicate with family MD	5	−0.73
Your recommendations will be followed under the care of the family MD	5	−1.77
Patient's perception that his/her family MD will be able to manage his/her thyroid cancer	5	−1.10
Your perception of the family MD's knowledge on how to adjust dose of levothyroxine	5	−1.19
Patient's lack of confidence in family MD's knowledge to adjust the dose of levothyroxine	4	−0.61
Lack of time to create a formal transitional care plan to give to family MD (i.e., much easier to just continue following)	3	−0.18
You do not want patients to feel you do not care about them if discharged from your practice	3	−0.11
Patients' lack of general understanding about their thyroid cancer and treatment plan	3	−0.23

The perceived factors were presented in the 8-item question on the participant study questionnaire, inquiring on the importance of these factors to discharging patients back to primary care physicians.

Qualitative responses

Among the 70 respondents, 51 (73%) provided a response to the open-ended question that inquired if there were any other factors or barriers that the respondent wanted to describe or elaborate in regard to transitioning the care of thyroid cancer patients to primary care physicians. Thematic saturation was achieved as determined by the study investigators. From the responses to the open-ended question, there were four main themes that emerged as factors affecting the decision to discharge: (i) primary care physician-related factors, (ii) patient-related factors, (iii) imaging-related factors, and (iv) guideline-related factors. As shown in Table 4, respondents commented on primary care physicians expressing a lack of confidence managing thyroid cancer follow-up, a lack of clarity if a primary care physician has knowledge on how to manage low-risk thyroid cancer, high rates of re-referral after patients were discharged, and patients not having a primary care doctor. This primary care-related theme was illustrated, for example, when a respondent stated “I have no idea what the comfort level of primary care doctors are—they can vary depending on their experience and practice” (P40). Another respondent shared that “Primary care physicians are rare to find and commonly unreliable, I will never consider leaving my cancer patients to primary care” (P1). Furthermore, one respondent highlighted that “Primary care physicians re-refer patients and insist they remain under endocrinology supervision” (P34).

Table 4.

Qualitative Data on Endocrinologist-Perceived Factors (Themes and Subthemes)

Themes	Subthemes
Primary care physician related	• Primary care physician has expressed a lack of confidence in managing thyroid cancer
	• Unclear if the primary care physician has knowledge on how to manage low-risk thyroid cancer
	• If discharged, there is a high rate of re-referral
	• Patient does not have a primary care doctor
Patient related	• Patient requests to be followed by an endocrinologist
Patient related	• Patients have anxiety about not being followed by a specialist
Imaging related	• Lack of universal high-quality ultrasound interpretation
Imaging related	• Nonspecific ultrasound findings common and unclear what to do in these cases
Guideline related	• Lack of knowledge on when to discharge
Guideline related	• No handouts to provide primary care physician or patient upon time of discharge

Patient-related factors included patients requesting to be followed by an endocrinologist or patients having anxiety about not being followed by a specialist. These factors were illustrated by a respondent who shared that “My main issue is that patients do not want to leave my practice even after I explain to them why it is okay” (P29). Moreover, another respondent mentioned that “Patients I've inherited from other endocrinologists who retired expect to be followed by an endocrinologist for the rest of their life” (P52).

Imaging-related factors focused on a lack of universal high-quality ultrasound interpretation and nonspecific ultrasound findings being common, resulting in a lack of clarity on what to do. For example, one respondent stated that a major issue was a “Lack of universal availability of high quality ultrasound interpretation” (P58). Another brought attention to the “concern about the ability to interpret nuances of the data and quality of imaging availability to primary care doctors” (P16).

Finally, guideline-related factors focused on a lack of knowledge on when to discharge and the lack of information provided to primary care physicians or patients upon time of discharge. These factors were evident when one respondent highlighted the importance of “appropriate guidelines/criteria to standardize practice for discharge across endocrinologists” (P46). In addition, another respondent said “I would welcome a structured discharge protocol that was supported by Cancer Care Ontario” (P64).

Discussion

This is the first known study reporting the views of endocrinologists regarding thyroid cancer follow-up care. In this study, the majority of endocrinologists agreed that certain patient populations required long-term specialist follow-up, particularly those with high-risk thyroid cancer, nonspecific cervical lymphadenopathy, recurrence of neck disease that was stable, and stable lung nodules. However, for other thyroid cancer patient populations, perceptions varied widely about discharging these patients to their primary care doctor. Although we cannot make any direct causal link through this study, the factors affecting the decision to discharge described by specialists may shed some light into why variation in discharge patterns exists.

Responses revealed that the majority of study participants lacked confidence in primary care follow-up because they were uncertain of primary care physicians' expertise in making medication changes or if primary care physicians would follow specialist recommendations. These findings are consistent with previous research of other cancer patient populations (6,17). Furthermore, the perceived factor that patients prefer specialist follow-up and lack trust in primary care physician follow-up is consistent with a study examining the perceptions of thyroid cancer survivors regarding follow-up care (21). Further research examining if structured education for primary care physicians or formalized transition programs for patients could help change these perceptions is needed. Currently in Canada, there are clinical programs in development or in operation that facilitate the transition of cancer patient care from specialist to primary care physician, and one such program has been established in the province of Ontario. The After Cancer Treatment Transition (ACTT) program at Women's College Hospital (Toronto, Canada) cares for recurrence-free patients who completed active treatment for melanoma, breast, gynecological, thyroid, testis, and colorectal cancer. Patients are followed up at ACTT for a variable period of time to be transitioned back to their primary care physicians safely and effectively. The ACTT program provides patients with postcancer care, which includes management of treatment side effects, surveillance for recurrence, planning for transition back to primary care, emotional support, and community resources.

Studies in other areas of oncology have failed to show differences in mortality benefit or time to detect disease when comparing specialist versus primary care physician follow-up for low-risk patients (7,8). However, this study highlights the difficulty in defining the role of the endocrinologist and primary care physician when it comes to low-risk thyroid cancer patients. The incidence and complexity of each cancer differ and there is concern that primary care physicians alone may not be best suited to follow these issues. A survey of primary care physicians in Western Canada found significant variation in follow-up care, with deviation from current American Thyroid Association (ATA) guidelines (22).

Thus, another area of interest that should be examined, given that it was a major factor stated by specialists, is the view of primary care physicians and their knowledge and comfort in managing thyroid cancer. They may be hesitant to provide thyroid cancer follow-up care due to lack of training or time/workload restrictions to provide adequate care. However, if this is the case, with updated recommendations, a structured follow-up plan from the specialist, and guidelines on when to re-refer, primary care physicians may become more confident in their ability to care for this patient population. There may be a need for updated thyroid cancer guidelines such as those from the ATA, to specifically address the follow-up of patients with low-risk thyroid cancer, including follow-up frequency, recommended laboratory tests, timing of neck ultrasound or other imaging, and criteria for referral back to the endocrinologist. In addition, there may be a need for consistent guidelines related to neck ultrasound interpretations and reporting so as to minimize ambiguity and interpretation by the ordering physician. Overall, studies from other oncology areas support the positive effects of preventive care and screening, as well as managing long-term cancer sequelae with better coordination of care between specialists and primary care physicians (23 –25).

It is common to see strong bonds form between oncology patients and specialists, with oncology survivorship studies revealing that these patients continue to rely on their specialist for medical expertise due to fear of disease recurrence (8). Considering patients highly trust their specialists, perhaps there is an opportunity for endocrinologists to educate and reassure their low-risk thyroid cancer patients that follow-up by a primary care physician (after five years if no recurrence) is an acceptable practice. The current study also suggests very different perceptions on the role of endocrinologist themselves such that some feel they should follow their patients continuously, while others believe the opposite. These different philosophies are deeply ingrained and represent challenges to standardizing transition practices. However, as the incidence of thyroid cancer increases, so has the clinical and economic burden on the health care system. Cost models have estimated the lifetime cost of a low-risk thyroid cancer patient to be $34,723 per patient (26). A recent study by Imran et al. comparing primary versus tertiary care follow-up of low-risk differentiated thyroid cancer further supports that follow-up by primary care doctors provides significant economic benefits to the health care system (15). Thus, understanding the balance between the increased cost, time pressures, and wait times of specialist care, with those who will significantly benefit from specialist care, is essential to improving the societal burden and clinical practice of caring for low-risk thyroid cancer patients (27).

This study had several limitations that need to be considered when interpreting the findings. First, the respondent rate for this study was 35.5%, slightly lower than the 50% ± 20% average for most surveys (28), however, this was due to efforts being made to recruit specialists across Ontario with differences in practice rather than only tertiary care centers. Nevertheless, the majority of respondents practiced in cities with a population of over 1 million. Ontario is a Canadian province with over 12 million people, with very diverse demographics so the data from this study have a strong potential to be generalizable since the region in general does not have a homogenous population. Although there is the possibility of selection bias as respondents who participated may still not be representative of specialists across Ontario, it should be noted that the demographics of respondents indicated that it was not skewed in sex (50% female, 45% male) or in years of practice (Table 1). Second, respondents who participated may have had a special interest in survivorship care, and thus, their responses may not be representative of all specialists. Last, for those questions with a wide range of responses, we were unable to do subgroup analysis to see if trends existed based on demographic data considering the sample size was small, data were collected anonymously, and minimal demographic information was collected to reduce the length of the survey and in turn optimize response rate. However, using qualitative responses did help provide a more complete understanding and context of perceived factors affecting the transition of patient care to primary care physicians. Moving forward, there is potential value in the following future work: (a) examining the perception of low-risk thyroid cancer patients in regard to primary care follow-up; (b) examining the perception of primary care physicians in regard to thyroid cancer patient follow-up; and (c) identifying the features of an effective model of follow-up/transition care.

Conclusion

There is a lack of confidence and willingness among endocrinologists to transition the care of thyroid cancer patients to primary care physicians even when patients are low risk or stable. A key factor was that endocrinologists perceived primary care physicians to lack knowledge and experience to manage the long-term care of thyroid cancer patients. However, endocrinologists are also not well informed that primary care physicians do monitor and care for stable cancer survivors. Overall, there is a need to provide clear, consistent, and accurate information to endocrinologists, primary care physicians, and thyroid cancer patients on postcancer treatment care, which may include implementing standard guidelines or protocols for discharge and allocating appropriate resources (i.e., imaging interpretation, expertise) to deliver long-term care.

Footnotes

Acknowledgments

We greatly appreciate the participation of the endocrinologists who completed the study survey.

Author Disclosure Statement

No competing financial interests exist.

Funding Information

This study was completed with no external funding. All contributing authors did not receive any funding.

References

Canadian Cancer Society (014 Canadian Cancer Statistics 2014, Provincial/Territorial Cancer Registries, Public Health Agency of Canada. Available at www.cancer.ca (accessed September 15, 2018 ).

Canadian Cancer Society 2019 Canadian Cancer Statistics. Government of Canada. Available at www.cancer.ca/∼/media/cancer.ca/CW/cancer%20information/cancer%20101/Canadian%20cancer%20statistics/Canadian-Cancer-Statistics-2019-EN.pdf?la=en (accessed January 10, 2020 ).

Topstad

, Dickinson

. 2017. Thyroid cancer incidence in Canada: a national cancer registry analysis. CMAJ Open, 5:612–616.

Cooper

, Doherty

, Haugen

, Kloos

, Lee

, Mandel

, Mazzaferri

, McIver

, Pacini

, Schlumberger

, Sherman

, Steward

, Tuttle

. 2009. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid, 19:1167–1214.

Baravelli

, Krishnasamy

, Pezaro

, Schofield

, Lotfi-Jam

, Rogers

, Milne

, Aranda

, King

, Shaw

, Grogan

, Jefford

. 2009. The views of bowel cancer survivors and health care professionals regarding survivorship care plans and post treatment follow up. J Cancer Surviv, 3:99–108.

Kantsiper

, McDonald

, Geller

, Shockney

, Snyder

, Wolff

. 2009. Transitioning to breast cancer survivorship: perspectives of patients, cancer specialists, and primary care providers. J Intern Med, 24 (Suppl 2):S459–S466.

Grunfeld

, Mant

, Yudkin

, Adewuyi-Dalton

, Cole

, Stewart

, Fitzpatrick

, Vessey

. 1996. Routine follow up of breast cancer in primary care: randomized trial. BMJ, 313:665–669.

Grunfeld

, Levine

, Julian

, Coyle

, Szechtman

, Mirsky

, Verma

, Dent

, Sawka

, Pritchard

, Ginsburg

, Wood

, Whelan

. 2006. Randomized trial of long-term follow-up for early- stage breast cancer: a comparison of family physician versus specialist care. J Clin Oncol, 24:848–855.

Sisler

, Brown

, Stewart

. 2004. Family physicians' roles in cancer care. Survey of patients on a provincial cancer registry. Can Fam Physician, 50:889–896.

10.

Grunfeld

, Fitzpatrick

, Mant

, Yudkin

, Adewuyi-Dalton

, Stewart

, Cole

, Vessey

. 1999. Comparison of breast cancer patient satisfaction with follow-up in primary care versus specialist care: results from a randomized controlled trial. Br J Gen Pract, 49:705–710.

11.

Morley

, Goldfarb

. 2015. Support needs and survivorship concerns of thyroid cancer patients. Thyroid, 25:649–656.

12.

Bresner

, Banach

, Rodin

, Thabane

, Ezzat

, Sawka

. 2015. Cancer-related worry in Canadian thyroid cancer survivors. J Clin Endocrinol Metab, 100:977–985.

13.

Schultz

, Stava

, Vassilopoulou-Sellin

. 2003. Health profiles and quality of life of 518 survivors of thyroid cancer. Head Neck, 25:349–356.

14.

Hyun

, Alhashemi

, Fazelzad

, Goldberg

, Goldstein

, Sawka

. 2016. A systematic review of unmet information and psychosocial support needs of adults diagnosed with thyroid cancer. Thyroid, 26:1239–1250.

15.

Imran

, Chu

, Rajaraman

, Ghosh

, De Brabandere

, Kaiser

, Van Uum

. 2019. Primary versus tertiary care follow-up of low-risk differentiated thyroid cancer: real-world comparison of outcomes and costs for patients and health care systems. Eur Thyroid J, 8:208–214.

16.

Cancer Care Ontario. 2018. Thyroid Cancer Pathway Map 2017. Available at www.cancercareontario.ca/en/pathway-maps/thyroid-cancer (accessed September 15, 2018 ).

17.

Virgo

, Lerro

, Klabunde

, Earle

, Ganz

. 2013. Barriers to breast and colorectal cancer survivorship care: perceptions of primary care physicians and medical oncologists in the United States. J Clin Oncol, 31:2322–2336.

18.

Braun

, Clarke

. 2014. What can “thematic analysis” offer health and well-being researchers?. Int J Qual Stud Health Well-being, 9:1–2.

19.

Bowen

. 2008. Naturalistic inquiry and the saturation concept: a research note. Qual Res, 8:137–152.

20.

Hsieh

, Shannon

. 2005. Three approaches to qualitative content analysis. Qual Health Res, 15:1277–1288.

21.

Bender

, Wiljer

, Sawka

, Tsang

, Alkazaz

, Brierley

. 2016. Thyroid cancer survivors' perceptions of survivorship care follow-up options: a cross-sectional, mixed-methods survey. Support Care Cancer, 24:2007–2015.

22.

Lam

, Strugnell

, Bajdik

, Holmes

, Wiseman

. 2013. Limited adequacy of thyroid cancer patient follow-up at a Canadian tertiary care centre. Can J Surg, 56:385–392.

23.

Snyder

, Frick

, Peairs

, Kantsiper

, Herbert

, Blackford

, Wolff

, Earle

. 2009. Comparing care for breast cancer survivors to non-cancer controls: a five-year longitudinal study. J Gen Intern Med, 24:469–474.

24.

Hewitt

, Bamundo

, Day

, Harvey

. 2007. Perspectives on post-treatment cancer care: qualitative research with survivors, nurses, and physicians. J Clin Oncol, 25:2270–2273.

25.

Hewitt

, Ganz

. 2007. Implementing Cancer Survivorship Care Planning-Workshop Summary. Washington, DC: The National Academies Press.

26.

Aschebrook-Kilfoy

, Brown

, Shih

, Kaplan

, Chiu

, Angelos

, Grogan

. 2013. The clinical and economic burden of a sustained increase in thyroid cancer incidence. Cancer Epidemiol Biomarkers Prev, 22:1252–1259.

27.

Mille

, Roy

, Carrère

, Ray

, Ferdjaoui

, Späth

, Chauvin

, Philip

. 2000. Economic impact of harmonizing medical practices: compliance with clinical practice guidelines in the follow-up of breast cancer in a French Comprehensive Cancer Center. J Clin Oncol, 18:1718–1724.

28.

Baruch

, Holtom

. 2008. Survey response rate levels and trends in organizational research. Hum Relat, 61:1139–1160.