Abstract
Context
Little is known about how patients’ emotions impact the choice between hemi- and total thyroidectomy (TT) for low-risk thyroid cancer (LR-TC) and how these emotions change after treatment.
Objective
To investigate thyroid cancer-specific fear and worry both before and after treatment of LR-TC with hemi- or TT.
Methods
This prospective cohort study enrolled adults with confirmed or likely LR-TC at 15 institutions. Participants completed measures of thyroid cancer-related fear and worry at the time of their treatment decision and 9 months later. Participants were categorized as having low, medium, or high levels of fear and worry in accordance with the literature. Those choosing hemithyroidectomy were compared to those choosing TT.
Results
Of 177 eligible patients, 125 (70.6%) enrolled and 114 completed both surveys (91.2% retention). Overall, 41 (36.0%) participants chose hemithyroidectomy and 73 (64.0%) chose TT. Across all participants, thyroid cancer-related fear and worry both decreased significantly after surgery (fear, 25.8 ± 6.4 to 23.1 ± 7.4; worry, 8.2 ± 2.4 to 5.4 ± 2.1, P < .001). The proportion of participants with high fear decreased from 64.9% to 50.9%, whereas the proportion with high worry decreased from 75.4% to 41.2% (P < .001 for both). At both time points, no differences existed between those choosing hemi- and TT in levels of worry or fear.
Conclusion
Patients with LR-TC report lower levels of fear and worry 9 months after surgery regardless of the extent of surgery, suggesting that both surgeries provide an emotional benefit to some patients. Thyroid cancer-related fear and worry do not appear to influence patients’ decisions to undergo hemi- or TT.
Keywords: thyroid cancer, longitudinal cohort, fear, worry
Most patients with differentiated thyroid cancer have a low risk of recurrence (1). According to the American Thyroid Association guidelines, either hemithyroidectomy (lobectomy) or total thyroidectomy are appropriate treatment options for low-risk differentiated thyroid cancers between 1 and 4 cm (2). Hemithyroidectomy has been shown to provide equivalent long-term survival and recurrence rates with reduced morbidity (3, 4). Patients have the opportunity to select a treatment option that best fit their needs, goals, and preferences, but the majority continue to undergo total thyroidectomy (5). As patients and their surgeons choose a treatment, emotions can heavily influence the extent of cancer surgery (6-8).
During decision-making, emotions such as fear and worry have the potential to influence a patient to select a treatment choice that provides the most perceived or anticipated emotional benefit (9-11). Although quantitative and qualitative data indicate that emotions affect a patient's choice between active surveillance and thyroidectomy for very small thyroid cancers measuring <2 cm, little is known about the influence of emotions on the choice between hemi- and total thyroidectomy or the way patients’ emotions vary over the course of their treatment (12-15). Additionally, patients’ levels of fear and worry may change to differing degrees depending on their surgical choice and extent of surgery.
This study sought to investigate the experience of patients with low-risk thyroid cancer with respect to disease-specific fear and worry both before and after their surgical treatment. We aimed to elucidate the potential differences in fear and worry levels for patients choosing 2 different index operations: hemi- or total thyroidectomy. An improved understanding of how thyroid cancer-related fear and worry are associated with treatment choice and how treatment affects these emotions will help clinicians support future patients during treatment decision-making for this disease. This information can also help guide the expectations of patients and clinicians in terms of the anticipated emotional benefits of treatment.
Methods
Participants and Settings
Patients with biopsy-proven papillary thyroid cancer, cytology suspicious for papillary thyroid cancer, or ≥70% risk of malignancy on molecular testing were recruited to participate in this prospective study at 15 institutions from November 2019 to June 2021. Eligible patients were age 18 years and older, had a thyroid nodule measuring ≤4 cm, were without clinical (palpable or ultrasound-detectable) or biopsy evidence of lymph node or distant metastasis, planning to undergo thyroid surgery, and had access to the internet. Patients were excluded if they chose active surveillance, had a history of thyroid cancer or thyroid surgery, had suspicious lymphadenopathy or evidence of extrathyroidal extension on imaging, did not speak English, and/or were considered vulnerable based on the Common Rule. The study was approved by the University of Wisconsin institutional review board.
Data Collection
At each study site, all eligible patients were identified, invited to participate by their surgeon, and given a study brochure with a unique participant ID and a URL to the study website (www.choicestudy.org). If eligible patients provided permission, their contact information was shared with the study team, which reminded patients about the possibility to enroll up to 3 times. To ensure eligibility, participants completed online screening questions before proceeding to an electronic consent. Because of the COVID-19 pandemic, accrual was slower than anticipated and halted at some sites during data collection. Participants completed 2 Qualtrics-based surveys: once after seeing their surgeon, but before having surgery, and another 9 months later. Participants received $5 preincentive, $30 for completing the first, and $40 for completing the second survey. Participants had 45 days to complete the second survey.
Measures
The survey instrument (Supplement 1) was developed by the study team and reviewed by experts in the field; it underwent cognitive testing with patients and was piloted before administration (16). Measures of the primary outcomes (fear and worry) were adapted minimally from validated breast cancer disease-specific fear and worry scales (17, 18). For each, the word “breast” was replaced with the word “thyroid.” In the Fear Scale, responses to 7 statements, each on a 5-point Likert scale ranging from strongly disagree (1) to strongly agree (5), were analyzed as an aggregate, continuous score. Responses were categorized and analyzed in a matter consistent with prior studies as having high (>23), moderate (16-23), or low (8-15) levels of fear. A higher score indicated a higher level of self-perceived fear. Thyroid cancer-specific anxiety was assessed with the State-Trait Anxiety Inventory, which assessed anxiety at a given time on a 5-point Likert scale (19). Higher scores indicate higher levels of anxiety.
Thyroid cancer-specific worry was assessed with 3 questions each on Likert scale (17). Questions asked if participants were worried about their thyroid cancer or nodule, how much their worry affected their mood, and how much their worry impacted their daily activities. Responses were summed and categorized in a matter consistent with the literature as having high (7-13), moderate (5-6), or low (3-4) levels of worry. To further examine survivors’ concerns at follow-up, participants completed (1) a 6-item, validated scale about worry related to health and (2) 2 previously published questions about their estimates of recurrence and death over 10 years (20-22). The impact of worry was measured using the worry impact index with 6 questions each on a 4-point Likert scale (17, 23). Additionally, respondents were asked about demographic information, including age, gender, race/ethnicity, and level of education. Clinical data were collected from patients about their surgical decision and complications, nodal metastasis, and cytology and pathology results.
Data Analysis
Descriptive statistics were performed for all variables. For comparisons, a complete case analysis was performed because of the low rate of missingness (<2%) and high rate of retention (>90%). One participant was excluded from analyses because they ultimately chose active surveillance. Differences in means between surgery groups were compared with independent samples t-tests. Changes in preoperative and postoperative scores, for the same patient, were evaluated using paired t-tests. Likewise, differences in proportions for surgery groups were compared with the Pearson chi-square and differences for the same patients were compared with the McNemar chi-square. A linear mixed model was used to confirm the results of the t-tests and a generalized estimating equation with a logit link, a logistic regression model for repeated measures, was used to confirm the chi-square tests for comparisons of high vs moderate/low levels of categorical variables. All analyses were performed using SAS statistical software (Version 9.4). Sankey plots were generated to depict individual changes in levels of fear and worry overtime using SankeyMATIC (https://sankeymatic.com/)
Because fear and worry were measured on different scales, we calculated power based on effect size. Given that 41 patients chose hemithyroidectomy and 73 selected total thyroidectomy, we have 72% power for a medium effect size (of 0.5) and 98% power for a large effect size (of 0.8), but only 17% power for a small effect size (of 0.2). The magnitude of effect size was estimated according to the Cohen guidelines for mean difference (24). To have clinical significance, an effect size should at least approach 0.5. For fear, a medium effect size of 0.5 corresponds to a shift of approximately 3.5. For worry, a medium effect size corresponds to a shift of 1.1.
Results
Demographics
Of 177 patients invited, 125 completed the initial survey (70.6% response) and 114 completed the 9-month follow-up (91.2% retention; Fig. 1). The age, race, and gender distribution was similar for those who chose hemithyroidectomy and those choosing total thyroidectomy (Table 1). Overall, 83.3% of participants identified as female, 82.5% were White, and 57.0% had received a bachelor's degree and/or graduate/professional degree (Table 1). Of the 114 participants, 41 (26.0%) chose hemithyroidectomy and 73 (64.0%) selected total thyroidectomy.
Figure 1.
CONSORT diagram of study enrollment and retention. AS, active surveillance.
Table 1.
Demographic and clinical data
| Characteristic | All (N = 114) |
Hemithyroidectomy (N = 41) |
Total thyroidectomy (N = 73) |
P |
|---|---|---|---|---|
| Age, mean (SD) | 45.6 (14.7) | 42.6 (13.0) | 47.3 (15.4) | .106a |
| Biological sex, n (%) | .097b | |||
| Female | 95 (83.3%) | 31 (75.6%) | 64 (87.7%) | |
| Male | 19 (16.7%) | 10 (24.4%) | 9 (12.3%) | |
| Race/ethnicity, n(%) | .084c | |||
| White | 94 (82.5%) | 31 (75.6%) | 63 (86.3%) | |
| Black/African American | 3 (2.6%) | 3 (7.3%) | 0 (0.0%) | |
| Hispanic or Latino | 2 (1.8%) | 0 (0.0%) | 2 (2.7%) | |
| American Indian/Alaska Native | 1 (0.9%) | 1 (2.4%) | 0 (0.0%) | |
| Asian | 11 (9.6%) | 5 (12.2%) | 6 (8.2%) | |
| Not listedd | 3 (2.6%) | 1 (2.4%) | 2 (2.7%) | |
| Highest level of education | .423c | |||
| Some high school or less | 2 (1.8%) | 0 (0.0%) | 2 (2.7%) | |
| High school graduate/GED | 10 (8.8%) | 4 (9.8%) | 6 (8.2%) | |
| Some college or associate's degree | 37 (32.5%) | 12 (29.3%) | 25 (34.2%) | |
| Bachelor's degree | 36 (16.7%) | 17 (41.5%) | 19 (26.0%) | |
| Graduate/professional degree | 29 (25.4%) | 8 (19.5%) | 21 (28.8%) | |
| Result of thyroid nodule biopsy | .398c | |||
| Papillary thyroid cancer | 76 (66.7%) | 25 (61.0%) | 51 (69.9%) | |
| Suspicious for papillary thyroid cancer | 29 (25.4%) | 11 (26.8%) | 18 (24.7%) | |
| Molecular testing with >70% risk of thyroid cancer | 5 (4.4%) | 2 (4.9%) | 3 (4.1%) | |
| Unsure | 3 (3.5%) | 2 (4.9%) | 1 (1.4%) | |
| Family history of thyroid cancer | .111c | |||
| Yes | 25 (21.9%) | 5 (12.2%) | 20 (27.4%) | |
| No | 79 (69.3%) | 31 (75.6%) | 48 (65.8%) | |
| Not sure | 10 (8.8%) | 5 (12.2%) | 5 (6.8%) | |
| Family/friend history of cancer | .034c | |||
| Yes | 99 (86.8%) | 32 (78.0%) | 67 (91.8%) | |
| No | 14 (12.3%) | 9 (22.0%) | 5 (6.8%) | |
| Not sure | 1 (0.9%) | 0 (0.0%) | 1 (1.4%) | |
| Family/friend died of cancer | .380c | |||
| Yes | 75 (75.8%) | 22 (68.8%) | 53 (79.1%) | |
| No | 22 (22.2%) | 9 (28.1%) | 13 (19.4%) | |
| Not sure | 2 (2.0%) | 1 (3.1%) | 1 (1.5%) |
Abbreviations: GED, General Education Diploma; TC, thyroid cancer.
a t-test.
b Pearson chi-square test.
c Fisher exact test.
d Race not listed: Croatian/Italian, Eurasian, South Asian/Indian, mixed race Asian and White.
Thyroid Cancer-related Fear and Worry at Time of Treatment Choice
At the time of the treatment decision, evaluation of thyroid cancer-related fear demonstrated no differences between patients choosing hemithyroidectomy and those selecting total thyroidectomy with respect to mean thyroid cancer-related fear score (25.1 ± 6.4 vs 26.1 ± 6.5; scale 8-40, P = .42) (Fig. 2). The proportion of participants with high levels of thyroid cancer-related fear (score of >23) was also similar between those who selected hemithyroidectomy and total thyroidectomy before treatment (58.5% vs 68.5%, P = .285).
Figure 2.
The differences in and changes between thyroid cancer-related fear (left) and worry (right) scores in those choosing hemithyroidectomy compared to total thyroidectomy before and after treatment. No differences were observed in fear or worry scores between those who chose hemithyroidectomy and total thyroidectomy at either time point. Fear and worry both decreased significantly within each group from the time of treatment decision to 9 months later (*P < 0.001).
Similarly, when we examined worry related to thyroid cancer at the time of the treatment decision, we again observed no differences between patients choosing hemithyroidectomy and total thyroidectomy (7.9 ± 2.4 vs 8.4 ± 2.5, respectively; scale 3-13, P = .34; Fig. 2). The impact of worry on participants’ mood and daily activities was also similar between the respective groups (4.4 ± 1.6 vs 4.7 ± 1.8, P = .40), as was their level of state anxiety (hemithyroidectomy 46.5 ± 13.2 vs total thyroidectomy 44.2 ± 13.2, P = .38. The proportion of patients with high levels of worry at the time of the treatment decision also did not differ based on treatment choice (hemithyroidectomy 73.2% vs total thyroidectomy 76.7%, P = .67). When we examined differences in fear and worry at the time of the treatment decision between sexes, race/ethnicity/gender, education, and treatment site, there were no significant differences in fear or worry. There were also no differences in fear and worry for those with family or friends having cancer or dying from cancer.
Thyroid Cancer-related Fear and Worry After Treatment
When reexamined after treatment, fear and worry remained similar between those who chose hemithyroidectomy and those who chose total thyroidectomy (fear, 23.3 ± 7.8 vs 23.0 ± 7.2, P = .85; worry, 5.3 ± 1.5 vs 5.4 ± 2.3, respectively, P = .85; Fig. 2). However, across all participants, comparison to presurgery levels revealed that thyroid cancer-related fear decreased from 25.8 ± 6.4 to 23.1 ± 7.4 (P < .001), whereas worry decreased from 8.2 ± 2.4 to 5.4 ± 2.1 (P < .001). The −2.7 change in thyroid cancer-related fear corresponded to a small to medium effect that may not have clinical significance. Meanwhile, the −2.8 change in worry indicates a large effect with clear clinically significance. Figure 2 shows that the statistically significant decrease in fear and worry over the study period was also observed when examined by treatment choice (P < .001 for both). When we examined differences in fear and worry after treatment between sex, race/ethnicity/gender, education, and treatment site, there were again no significant differences (fear, P = .249; worry, P = .260). Similarly, none of the emotional outcomes differed by family of friends having cancer or dying from cancer.
In addition, the proportion of participants with high levels of fear decreased from 64.9% to 50.9%, whereas the proportion of those with high levels of worry decreased from 75.4% to 41.2% (P < .001; Fig. 3). Changes in fear and worry levels for each participant are shown in Fig. 3. Significant decreases in the level of high negative emotions were observed in patients regardless of their treatment choice. For high levels of fear, patients who chose hemithyroidectomy decreased from 58.5% to 51.2% and those choosing total thyroidectomy decreased from 68.5% to 50.7% (P < .001 for both). For high levels of worry, those who chose hemithyroidectomy decreased from 73.2% to 22.0%, whereas those who selected total thyroidectomy decreased from 76.7% to 21.9% (P < .001) for both. Participants whose fear and worry increased from the low (n = 3) or moderate (n = 16) levels into the high level tended to have higher rates of nodal metastases identified intraoperatively (44.4%, n = 8) compared to patients who did not (23.9%, n = 23; P = .09).
Figure 3.
The Sankey diagrams depict the change in individual levels of thyroid-cancer related fear (left) and worry (right) from the time of the treatment decision “presurgery” to their 9-month follow-up.
Further examination of survivors’ concerns at the 9-month follow-up demonstrated no differences between treatments regarding participants’ levels of worry about future diagnostic tests, other cancers, thyroid cancer recurrence, dying, their health, or their children's health (Supplement 2) (25). In addition, the proportion who overestimated their 10-year risk of recurrence and death was similar between all participants, with 33.6% overestimating recurrence and 14.2% overestimating mortality.
Discussion
Regardless of chosen treatment decision, whether hemi- or total thyroidectomy, patients with clinically low-risk thyroid cancer or high preoperative suspicion of thyroid cancer reported similar levels of thyroid cancer-related fear and worry at the time of diagnosis. These levels of fear and worry decreased significantly over the 9-month time frame as did the proportion of patients with high levels of fear and worry. Based on these results, surgical treatment of low-risk thyroid cancer with either hemithyroidectomy or total thyroidectomy provides an emotional benefit to some patients. However, considerable proportions of patients still had high levels of fear and worry even after completing treatment and recovery (50.9% and 41.2%, respectively). These findings are reflected in patients with breast cancer, in which despite completion of treatments, there is a high prevalence of moderate and severe fear (53% and 30%, respectively), specifically in relation to fear of recurrence (26). When taking effect size into consideration, the clinical significance of these change are great for thyroid cancer-related worry that for fear.
Prior studies support our finding that patients with low-risk thyroid cancer experience persistent negative emotions like fear and worry posttreatment, although our study is the first we know of to show that these are decreased compared to presurgery levels (27, 28). A cross-sectional study of thyroid cancer survivors with a favorable prognosis who were 2 to 4 years posttreatment demonstrated that worry about recurrence persists after treatment, especially among vulnerable groups with lower education or younger age (29, 30). Similar to our data, these authors found no difference in worry by extent of surgery. For all cancers, worry about recurrence can persist for years after treatment. The risk of recurrence can be particularly challenging for survivors of thyroid cancer who can experience recurrence 30 or 40 years later (29, 31). Despite the propensity for worry to linger, it is not surprising that thyroid cancer-related fear and worry both decrease in the early postoperative course. However, the finding that these emotions decrease to a similar degree regardless of the extent of surgery is new and significant, especially given data that suggest emotions impact treatment preference for this disease (12-14).
Recent data about the choice for surgery or active surveillance in patients with a very low risk of recurrence provide additional insight into the association between emotions and treatment choice. A study by Ho et al showed that patients with thyroid cancer measuring <2 cm who chose immediate surgery had higher baseline levels of thyroid cancer-specific anxiety compared to patients who chose active surveillance (15). The comparatively higher anxiety scores for patients who chose immediate surgery persisted over the 4-year study period when compared to those who chose surveillance despite surgical intervention. The thyroid cancer-specific anxiety also did not decrease significantly in the first year after surgery. Similarly, a study by Sawka et al showed that patients with <2 cm papillary thyroid cancer who had greater fear of thyroid cancer progression were more likely to select surgical treatment over active surveillance (14). Both studies show that heightened negative emotions like anxiety and fear influence decision-making in thyroid cancer treatment and are associated with a preference for surgery rather than active surveillance (14). However, our results suggest that these emotions may not be a significant driver of the extent of the surgery. Prior related work by our group does indicate that where a patients is treated may affect the decision to undergo total or hemithyroidectomy (32).
Despite fear and worry decreasing after treatment, patients with thyroid cancer, especially those with higher baseline levels, may need additional support to reduce fear and worry before treatment and decision making. For patients with thyroid and other types of cancer, cognitive behavioral therapy and other forms of psychotherapy are evidence-based, nonpharmacological treatments with demonstrated clinical efficacy. A study by Javaloyes et al examining the effect of counseling patients with differentiated thyroid cancer after a total thyroidectomy showed a statistically significant reduction in anxiety compared to the control (33). This intervention could be adapted for the pretreatment period. A meta-analysis by Osborn et al demonstrated that cognitive behavioral therapy for adult cancer survivors was linked to the short-term reduction of depression and anxiety (34). Another intervention increasingly integrated into oncological treatment is mindfulness-based cognitive therapy, which has been shown to reduce symptoms of anxiety for patients with cancer for at least 3 months following intervention (35). Even more basic interventions, such as changing the terminology used to describe masses from cancer to lesion, may reduce emotional distress in patients with thyroid cancer and have a meaningful impact on the treatment decision making process (36, 37). For example, use of the term “thyroid conserving surgery” in place of “hemithyroidectomy” may promote uptake of this less extensive procedure.
Although the results of this longitudinal cohort are important to help guide treatment decision-making and anticipated emotional outcomes, this study has limitations to consider. First, there is a risk for recall bias because outcomes were self-reported by patients. Second, most patients were treated at large academic centers, which potentially limits generalizability. However, patients were recruited from 15 different institutions with diverse geography and patient populations. In addition, there were no differences in emotional scales, treatment chosen, and treatment received by site. Because some institutions had COVID-19-related restrictions and/or halted study accrual, selection bias or sampling errors may have affected the results. Another limitation is that the scales used to assess fear and worry were adapted from breast cancer measures and may have different properties in a thyroid cancer population, although both the fear (Cronbach α = .91) and worry scales (Cronbach α = .83) demonstrated strong reliability (38). Furthermore, our study may not reflect all the other factors that influenced decision making for operative treatments, such as surgeon preference and recommendation. Nonetheless, these are the first longitudinal data to our knowledge on disease-specific fear and worry after thyroidectomy in patients with thyroid cancer.
Conclusions
A majority of patients with low-risk thyroid cancer experience high levels of thyroid cancer-related fear and worry following diagnosis. Both fear and worry appear to decrease over time regardless of the extent of thyroidectomy, suggesting that removing the cancer provides an emotional benefit to some patients. Because these emotions do not appear to influence the chosen extent of surgery for this disease and oncologic outcomes are equivalent, further data are needed to investigate the factors that drive these decisions to best understand how to uphold patients’ values and preferences in treatment decision-making. Our findings open the possibility that interventions delivered early in the diagnostic process to reduce negative emotions, such as worry or fear, may improve the overall psychosocial well-being and long-term outcomes of patients.
Acknowledgments
The authors acknowledge the site lead surgeons and institutions who identified eligible patients: Priya Dedhia, MD, PhD—The Ohio State University; Matthew Nehs, MD—Brigham & Women's Hospital; Maria Bates, MD—Swedish American Hospital; Tammy Holm, MD, PhD—University of Cincinnati; Antonia Stephen, MD—Massachusetts General Hospital; Brenessa Lindeman, MD, MEHP—University of Alabama at Birmingham; Reese Randle, MD—Wake Forest University; and Benjamin James, MD—Beth Israel Deaconess Medical Center.
Contributor Information
Stephanie S Lee, Department of Surgery, University of Michigan, Ann Arbor, MI 48109, USA.
Alexis G Antunez, Department of Surgery, Brigham and Women's Hospital, Boston, MA 02115, USA.
Brandy Sinco, Department of Surgery, University of Michigan, Ann Arbor, MI 48109, USA.
Megan C Saucke, Department of Surgery, University of Wisconsin-Madison, Madison, WI 53706, USA.
Kyle J Bushaw, Department of Surgery, University of Wisconsin-Madison, Madison, WI 53706, USA.
Sophie Dream, Department of Surgery, Medical College of Wisconsin, Milwaukee, WI 53226, USA.
Abbey Fingeret, Department of Surgery, University of Nebraska, Omaha, NE 68182, USA.
Masha J Livhits, Department of Surgery, University of California-Los Angeles, Los Angeles, CA 90095, USA.
Aarti Mathur, Department of Surgery, Johns Hopkins University, Baltimore, MD 21218, USA.
Alexandria D McDow, Department of Surgery, Indiana University, Indianapolis, IN 46202, USA.
Sanziana Roman, Department of Surgery, University of California—San Francisco, San Francisco, CA 94143, USA.
Corrine I Voils, Department of Surgery, University of Wisconsin-Madison, Madison, WI 53706, USA; Department of Surgery, William S. Middleton Memorial Veterans Hospital, Madison, WI 53705, USA.
Susan C Pitt, Department of Surgery, University of Michigan, Ann Arbor, MI 48109, USA.
Funding
This study was supported by the National Cancer Institute award K08CA230204 (PI, S.C.P.). S.C.P. is also supported by the National Cancer Institute award R03CA283105. A.G.A. is supported by the National Cancer Institute Training Program award T32 CA009672. A.M. is funded by the National Institute of Aging award R01AG076834. C.I.V. is funded by a Research Career Scientist award (RCS 14-443) from the VA Health Systems Research. The views are those of the authors and not of the U. S. Government.
Disclosure
No potential conflicts of interest were reported.
Data Availability
The data sets produced through the current study are not publicly available but are available from the corresponding author on reasonable request.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data sets produced through the current study are not publicly available but are available from the corresponding author on reasonable request.
