Abstract
Objective:
Nonmelanoma skin cancer (NMSC) is one of the most diagnosed cancers in the world, with the number of new occurrences rising every year. Most patients with facial skin cancer experience cancer-related worry. Yet, little is known about their worry during the period after cancer treatment. This study aimed to assess the long-term change of cancer worry after surgical treatment in patients with NMSC.
Methods:
Patients undergoing surgery for facial NMSC between December 2017 and March 2020 were asked to complete the FACE-Q Skin Cancer—Cancer Worry scale before (baseline), 3-month, and 1-year post-surgery.
Results:
A total of 151 patients completed the baseline and 3-month, and 99 (65.6%) the 1-year post-operative survey. A significant decrease in cancer worry score was seen between baseline and 3-month post-surgery (p < 0.001). No difference was found between the 3-month and 1-year post-surgery scores (p = 0.78). Less improvement in cancer worry was seen for patients who had one facial skin cancer in their medical history (p = 0.001) and patients who had a history of facial surgery (p < 0.001).
Conclusion:
Post-surgery patients still experience cancer worry. Therefore, targeted counseling might be of value when coping with cancer-related concerns. Patients with a history of facial NMSC and patients with a history of facial surgery might benefit from additional counseling.
Keywords: cancer worry, Mohs micrographic surgery, nonmelanoma skin cancer, oncology, patient reported outcome, psycho-oncology
1 |. BACKGROUND
Worldwide, nonmelanoma skin cancer (NMSC) is known as one of the most common cancers.1 Between 2 and 3 million cases of NMSC occur each year and the incident rates keep rising.2 Most NMSCs are located on the head and neck due to the high sun exposure in these areas.3,4 There are different treatment approaches for NMSC (e.g., excision, radiotherapy, anti-cancer creams), of which Mohs micrographic surgery (MMS) is increasingly being used for facial NMSC.5–7
Once diagnosed with NMSC, most patients experience cancer-related worry (e.g., worry about skin cancer progression).8 At first, removal of the skin cancer seems to result in lower levels of cancer worry.9 However, some cancer worry may persist due to factors that stay present after surgery; such as surgery-induced scarring.10,11 This may be a constant physical reminder of the skin cancer, resulting in an increased level of worry about their NMSC and the risk of new skin cancers. Patients with a history of skin cancer will have a lifelong risk of subsequent NMSC development.12 The estimated 3-year risk of new NMSCs lies between 18% and 44% and is shown to rise according to the number of prior occurrences in the medical history.13–16 This constant risk may ultimately worsen patients’ cancer worry as a fear of recurrence often develops once diagnosed with NMSC.17–19 Therefore, it is crucial for healthcare professionals to recognize patients’ cancer-related concerns and respond adequately to their need for supportive care.18
Although studies discussing skin cancer worry exist,8,9,17,18 there is little known on the long-term change of the cancer worry after facial NMSC treatment. More knowledge on cancer worry scores following surgery and cancer worry scores in different patient groups may help identify patients at risk for high cancer worry and those who may benefit from supportive care interventions. This study aimed to prospectively analyze cancer worry in patients before and after facial MMS for NMSC, with the use of the FACE-Q Skin Cancer Module, a validated patient-reported outcome measure specifically designed for patients undergoing facial skin cancer resection.20–22
2 |. METHODS
Institutional review board approval was obtained from Catharina Hospital, Eindhoven. A single-center prospective study design was used. Patients were enrolled at the Department of Dermatology between April 2017 and March 2020 and were asked to participate before undergoing MMS for NMSC. Informed consent was given prior to answering the survey. The reconstruction following MMS was performed either at the same department or at the Department of Plastic, Reconstructive, and Hand Surgery in the same hospital. Patients were included if they were 18 years or older, adequately fluent in the Dutch language, and available by email or phone. Information was given both verbally and through leaflets discussing the preparations, procedure, possible complications, and the follow-up period.
Electronic medical records were used to obtain relevant demographics and clinical information, such as the number of prior-facial and/or non-facial NMSC in the medical history, lesion size, lesion location, wound closure, any prior facial surgery (e.g., skin cancer, benign lesion removal, surgery because of trauma) and cancer history other than NMSC (e.g., prostate cancer, lung cancer, melanoma). The location of the lesion was categorized as (i) central: the eye, nose, and lips (ii) peripheral: forehead, scalp, cheek, chin, and ears. Wound closure techniques were divided into primary closure, flaps, and others (e.g., second intention healing and full-thickness skin graft [FTSG]). The longest diameter of the lesion after resection and before the reconstruction, in any axis, was termed “lesion diameter” and divided into two groups: <1.5 cm and ≥1.5 cm. Complications were recorded if surgical (e.g., ectropion repair) or non-surgical (e.g., administration of antibiotics) intervention by a medical healthcare professional was necessary.
2.1 |. Questionnaire
The FACE-Q Skin Cancer consists of five scales and two checklists. Each scale and checklist can be used independently or in conjunction with other scales and checklists. For this study the FACE-Q Skin Cancer—Cancer Worry scale was used. All patients received the validated Dutch translation of the questionnaire via mail prior to (baseline), 3-month, and 1-year after MMS.20–23 Questionnaires were considered complete when all items of the Cancer Worry scale were answered. Patients were included in the study if they completed the Cancer Worry scale at baseline and 3-month post-operative. The Cancer Worry scale consists of 10 questions on a Likert-type scale covering subjects such as general worry about skin cancer, worry cancer might spread, daily cancer worry, and anxiousness. Answer options were strongly disagree, disagree, agree, or strongly agree. The sum of the score was converted into a Rasch score ranging from 0 to 100.24 Higher scores indicate more cancer worry.
2.2 |. Statistical analysis
The differences between the cancer worry scores at baseline were calculated for the demographic and clinical variables. Non-normal distributed data, measured with the Shapiro Wilk test and Levene’s test, were tested with the Mann–Whitney U or Kruskal–Wallis H test; otherwise, the unpaired t-test or analysis of variance was applied. The Friedman test for non-normal distributed data was used to present differences in cancer worry scores per patient over time. Pairwise comparisons were performed with a Bonferroni correction for multiple comparisons. Statistical significance for this test was accepted at p < 0.017 level. The course of the mean cancer worry score was analyzed for associations with clinical and demographic characteristics by using a mixed linear regression model. A random intercept and slope were incorporated for every patient to measure improvement in cancer worry compared to baseline, with an adjustment for the baseline cancer worry score. Further analysis was done on the difference in cancer worry score between two timepoints by executing separate linear regression models for characteristics that showed significant associations with the cancer worry score. A p < 0.05 was considered statistically significant. Data management and analysis were performed using IBM SPSS statistics 26.0 (IBM).
3 |. RESULTS
A total of 239 patients completed the Cancer Worry scale before MMS. Of these patients, 151 completed the 3-month post-operative questionnaire and were therefore included in this study. The 1-year post-operative survey was completed by 99 (65.6%) patients. No significant difference was found between the included patients and the patients that only completed the baseline Cancer Worry scale (p = 0.48). In addition, no clinical or demographic differences were found between the lost to follow-up patients at 3-month versus baseline (n = 151 vs. n = 88) and 1-year versus 3-month (n = 99 vs. n = 52). The mean age at the time of surgery was 67.1 ± 11.7 years (mean ± standard deviation). Ninety-three patients (61.6%) had a central lesion and 58 (38.4%) a peripheral lesion. The mean size of the lesion was 1.6 ± 0.8 cm. Most patients were reconstructed with a primary closure (n = 74, 49.0%), followed by flap reconstruction (n = 58, 38.4%). Ten patients (6.6%) experienced a complication (flap reconstruction n = 4, primary closure n = 3, FTSG n = 3). All complications were minor, requiring surgical or non-surgical intervention (e.g., correction of ectropion, administration of antibiotics).
Most patients (92.7%, RASCH score range from 6 to 92) expressed some degree of cancer worry at baseline. Of the 151 patients, 27 patients (17.9%) had at least 1 other cancer diagnosis in their medical history (either current, in remission, or history of cancer, e.g., prostate cancer, lung cancer, melanoma). No significant difference in cancer worry was found between the 27 patients with a cancer diagnosis other than NMSC in their medical history and the 124 patients without a cancer diagnosis other than NMSC (n = 27, mean 34.0 ± 19.2 vs. n = 124, mean 37.1 ± 19.1, p = 0.34). Patients who had a history of prior facial surgery showed a higher cancer worry score compared to patients who did not (p = 0.03). From the patients with a history of prior facial surgery, 51 patients (80.9%) had undergone surgery for NMSC (mean cancer worry score 37.5 ± 17.9) and 12 patients (19.1%) had undergone a cosmetic (e.g., eyelid correction) or traumatic facial surgery (mean cancer worry score 50.3 ± 16.7). Baseline cancer worry scores, patient demographic and clinical variables are shown in Table 1.
TABLE 1.
Demographic and clinical characteristics by baseline cancer worry scores
| Variables | N (%) | Baseline cancer worry score, mean (SD) | p-Value |
|---|---|---|---|
| Age, years | |||
| <70 | 77 (51.0) | 36.5 (19.7) | 0.93a |
| ≥70 | 74 (49.0) | 36.6 (18.5) | |
| Gender | |||
| Male | 68 (45.0) | 33.9 (19.0) | 0.18a |
| Female | 83 (55.0) | 38.7 (18.9) | |
| Smoking | |||
| Yes/former | 88 (58.3) | 36.5 (19.0) | 0.94a |
| No | 63 (41.7) | 36.6 (19.4) | |
| Location lesion | |||
| Central | 93 (61.6) | 37.5 (19.3) | 0.37a |
| Peripheral | 58 (38.4) | 35.1 (18.9) | |
| Lesion diameter, cm | |||
| <1.5 | 78 (51.7) | 37.3 (19.4) | 0.64 |
| ≥1.5 | 73 (48.3) | 35.8 (18.8) | |
| Wound closure | |||
| Primary closure | 74 (49.0) | 35.4 (20.1) | 0.58a |
| Flap | 58 (38.4) | 37.2 (18.6) | |
| Othersb | 19 (12.6) | 39.2 (17.0) | |
| Number of prior facial NMSC | |||
| 0 | 92 (60.9) | 35.9 (20.0) | 0.67a |
| 1 | 39 (25.8) | 37.3 (18.2) | |
| ≥2 | 20 (13.3) | 38.4 (17.1) | |
| Number of prior non-facial NMSC | |||
| 0 | 105 (69.5) | 35.9 (20.2) | 0.54a |
| 1–2 | 20 (3.13) | 36.6 (16.4) | |
| ≥3 | 26 (17.2) | 39.4 (16.5) | |
| History of facial surgery | |||
| Yesc | 63 (41.7) | 40.0 (18.3) | 0.03a |
| No | 88 (58.3) | 34.1 (19.4) | |
Abbreviations: cm, centimeter; NMSC, nonmelanoma skin cancer; SD, standard deviation.
p-Value calculated with the Mann–Whitney U or Kruskall–Wallis H test.
Second intention healing, n = 6; full-thickness skin graft, n = 13.
Cosmetic (e.g., eyelid correction) or traumatic surgery n = 12, facial NMSC surgery n = 51.
During the 1-year follow-up period, the difference in cancer worry scores was statistically significant over time (p < 0.001). A significant decrease in cancer worry score was seen between baseline (mean 36.6 ± 19.1) and 3-month post-surgery (mean 27.3 ± 21.4, p < 0.001), and between baseline and 1-year post-surgery (mean 24.5 ± 19.5, p < 0.001). No significant difference in cancer worry score was found between 3-month and 1-year post-surgery (p = 0.78) (Figure 1). At the 3-month time point, the cancer worry score of the 52 patients who did not complete the 1-year post-operative survey did not significantly differ from the 99 patients that did complete the 1-year post-operative survey (n = 99 mean 25.3 ± 19.2 vs. n = 52 mean 31.1 ± 24.7, p = 0.19).
FIGURE 1.
The mean cancer worry score at each timepoint. Vertical lines indicate 95% confidence intervals
Results of the mixed linear regression model can be found in Table 2. This analysis revealed less improvement in cancer worry scores for patients who had a history of one prior NMSC compared to no history (p = 0.001, Figure 2). A history of two or more prior facial NMSC did not have an effect on change in cancer worry over time (p = 0.12). The change in cancer worry scores after treatment was greater in patients who did not have a history of facial surgery compared to patients who had a history of facial surgery (p < 0.001). No significant difference in cancer worry scores and the other patient characteristics were seen (see Table 2). A separate linear regression model demonstrated a significant difference in cancer worry score between baseline and 3-month post-operative for patients with one prior facial NMSC (p = 0.01, Figure 2) and patients with prior history of facial surgery (p = 0.01, Figure 2).
TABLE 2.
Summary of the mixed linear regression models on the cancer worry scores
| Estimate | Standard error | p-value | |
|---|---|---|---|
| Age, years | |||
| ≥70 (reference) | 0 | 0 | - |
| <70 | 0.32 | 2.66 | 0.91 |
| Timepoints | |||
| Three months (reference) | 0 | 0 | - |
| One year | −0.91 | 1.38 | 0.51 |
| Baselinea | 0.65 | 0.07 | <0.001 |
| Gender | |||
| Female (reference) | 0 | 0 | - |
| Male | 4.04 | 2.66 | 0.13 |
| Timepoints | |||
| Three months (reference) | 0 | 0 | − |
| One year | −0.89 | 1.38 | 0.52 |
| Baselinea | 0.66 | 0.07 | <0.001 |
| Smoking | |||
| Yes/former (reference) | 0 | 0 | - |
| No | −1.27 | 2.69 | 0.64 |
| Timepoints | |||
| Three months (reference) | 0 | 0 | - |
| One year | −0.90 | 1.38 | 0.51 |
| Baselinea | 0.65 | 0.07 | <0.001 |
| Location lesion | |||
| Peripheral (reference) | 0 | 0 | - |
| Central | 1.05 | 2.73 | 0.70 |
| Timepoints | |||
| Three months (reference) | 0 | 0 | - |
| One year | −0.90 | 1.38 | 0.52 |
| Baselinea | 0.65 | 0.07 | <0.001 |
| Lesion diameter, cm | |||
| ≥1.5 (reference) | 0 | 0 | - |
| <1.5 | 0.28 | 2.66 | 0.92 |
| Timepoints | |||
| Three months (reference) | 0 | 0 | - |
| One year | −0.91 | 1.38 | 0.51 |
| Baselinea | 0.65 | 0.07 | <0.001 |
| Wound closure | |||
| Others (reference) | 0 | 0 | - |
| Primary closure | 0.89 | 4.24 | 0.84 |
| Flap | −0.14 | 4.35 | 0.97 |
| Timepoints | |||
| Three months (reference) | 0 | 0 | - |
| One year | −0.92 | 1.38 | 0.51 |
| Baselinea | 0.65 | 0.07 | <0.001 |
| Number of prior facial NMSC | |||
| No (reference) | 0 | 0 | - |
| 1 | 10.32 | 3.02 | 0.001 |
| ≥2 | 6.12 | 3.86 | 0.12 |
| Timepoints | |||
| Three months (reference) | 0 | 0 | - |
| One year | −0.78 | 1.38 | 0.57 |
| Baselinea | 0.64 | 0.07 | <0.001 |
| History of facial surgery | |||
| Yes (reference)b | 0 | 0 | - |
| No | −9.98 | 2.60 | <0.001 |
| Timepoints | |||
| Three months (reference) | 0 | 0 | - |
| One year | −0.77 | 1.38 | 0.58 |
| Baselinea | 0.61 | 0.07 | <0.001 |
Abbreviations: cm, centimeter; NMSC, nonmelanoma skin cancer.
Cancer worry scores prior to surgery.
Cosmetic (e.g., eyelid correction) or traumatic surgery n = 12, facial NMSC surgery n = 51.
FIGURE 2.
The mean cancer worry score at each timepoint by patient characteristics. Vertical lines indicate 95% confidence intervals. The average cancer worry score at each point in time by (A) number of prior facial nonmelanoma skin cancer, (B) history of facial surgery, and (C) gender
4 |. DISCUSSION
Cancer worry can significantly impact patients’ well-being and increase their psychosocial distress, resulting in a decreased quality of life.17 This study showed that most patients experience varying levels of cancer worry when diagnosed with NMSC. These cancer worry levels decrease after treatment, which is consistent with previous study findings.9 A further decrease was observed until 1 year after MMS. However, post-surgery patients still experienced cancer worry. Some level of cancer worry could be beneficial as it might motivate patients to take preventative measurements for skin cancer (e.g., sunscreen). Nonetheless, fear might cause psychosocial complaints.17 Therefore, it is important to understand the patients’ concerns following diagnosis and treatment to prevent unnecessary fears, such as fear of dying from NMSC skin cancer as NMSC is known for having a low morbidity and mortality rate.12 As such, targeted counseling would help patients cope with their fears and thereby contribute to a successful recovery.18,25
In this study, patients without a history of facial skin cancer showed a larger decrease in cancer worry post-surgery compared to patients with a history of facial NMSC. The difference in cancer worry levels after surgery may be due to the prior skin cancer contributing to concerns about recurrence or the potential for new lesions, which is a common cause for concern among patients with NMSC.11,17 In this context, informing patients that the 5-year recurrence rates are considerably lower after MMS treatment compared to other treatment modalities could help decrease patients’ concerns.7,26 However, it is important to inform patients that the risk of new NMSC will continue to persist and that it may be useful to lower this risk with preventative measurements, for example, regular skin examination, sun protection, or more innovative methods such as smartphone applications and teledermoscopy.16,27–32 Therefore, this group of patients might benefit from receiving additional counseling and information on recurrence rates, future skin cancer risk, and skin cancer prevention.
Furthermore, patients that did not undergo facial surgery prior to treatment demonstrated a larger decrease in cancer worry after MMS than patients with a history of facial surgery. Visible facial scarring might result in worry about additional alterations and may thereby increase the fear of undergoing skin cancer treatment.25 Counseling and guidance could help these patients to go through the process of adapting to visible alterations25; such as showing the lesion before reconstruction, which may result in lower appearance-related distress.33
4.1 |. Study limitations
There are some limitations to this study. The study did not report on social support (e.g., relationship status, loneliness, and work environment) and did not register new facial NMSC diagnoses during the follow-up period. These factors may contribute to the cancer worry scores post-surgery. In addition, only patients who completed the baseline and 3-month post-operative time points were included, of which 65.5% of the patients completed all three time points; it is possible that those who refused to participate or did not complete the study had more or less cancer worry after 1 year. However, no significant difference was found between patient characteristics and cancer worry scores of the patients who were lost to follow-up and those who completed the study. Larger multicenter studies, including different skin cancer types, treatment types and patients’ social support, may bring a better understanding on cancer worry levels for patients diagnosed with NMSC. Furthermore, larger studies could also give more insight into the differentiation between any worry and clinical worry and the nature of the patients’ concerns.
4.2 |. Clinical implications
The outcome of this study could offer physicians a better understanding of cancer worry after treatment and may help specific patient groups better cope with their skin cancer. By incorporating the FACE-Q Skin Cancer—Cancer Worry scale in clinic, unchanged or increased levels of cancer worry can be detected over time. In addition, the physician could look at the individual items of the scale to differentiate between the cause of the cancer worry. This way, the Cancer Worry scale might identify patients who may benefit from targeted counseling or specialized psychological care. It may also result in fewer post-surgery visits for patients that do not need additional support. Consequently, incorporating the FACE-Q Skin Cancer—Cancer Worry scale in clinic might improve the quality and the efficiency of patient care.
5 |. CONCLUSION
After MMS treatment for facial NMSC, patients experience less cancer worry compared to baseline. However, for most patients, cancer worry was still present at 1-year post-surgery. Counseling may help patients cope with their cancer-related worry. Additionally, patients with a history of facial NMSC and a history of facial surgery might benefit from targeted counseling.
ACKNOWLEDGMENT
This article has no funding source.
Footnotes
CONFLICT OF INTEREST
The FACE-Q Skin Cancer Module is owned by Memorial Sloan-Kettering Cancer Center.
ETHICAL APPROVAL
Reviewed and approved by Catharina Hospital Eindhoven, The Netherlands. Approval, niet-WMO W17.037. Informed consent was given prior to answering the survey.
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.
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Associated Data
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Data Availability Statement
The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.