Abstract
Background:
With comparable overall survival and local recurrence rates with mastectomy, breast-conserving surgery (BCS) has become the cornerstone of therapy for breast cancer; however, the difference in the incidence of suicide between BCS and mastectomy among breast cancer survivors remains unclear. This study evaluated the mortality risk from suicide among breast cancer survivors and compared suicide risk between BCS and mastectomy using a population-based cohort.
Materials and methods:
Female patients newly diagnosed with first primary breast cancer, recorded in the Surveillance, Epidemiology and End Results database, were included. Standardized mortality ratio (SMR) and cumulative mortality rate from suicide among those who underwent BCS and mastectomy were compared.
Results:
A total of 1 190 991 patients with newly diagnosed first primary breast cancer were included in the study, of whom 56.5% underwent BCS and 36.1% underwent mastectomy. During the follow-up period, 667 suicides were recorded. Patients who underwent mastectomy exhibited significantly higher suicide mortality than the general population [mortality rate, 8.16 per 100 000 person-years; SMR 1.18 (95% CI 1.05–1.33)], while there was no significant difference in suicide rate between patients who underwent BCS and the general population [SMR 0.92 (95% CI 0.83–1.02)]. Multivariate Cox analysis revealed that BCS, compared with mastectomy, was associated with a significantly decreased risk of suicide among females with breast cancer [hazard ratio 0.80 (95% CI 0.68–0.95); P = 0.009].
Conclusion:
BCS was associated with a significantly lower incidence of suicide among females with breast cancer. BCS offers a compelling option for improving the quality of life and self-esteem of patients with cancer and provides a novel perspective on cancer management.
Keywords: breast-conserving surgery, suicide, breast cancer, mastectomy
Introduction
Highlights
The suicide risk after breast-conserving surgery (BCS) remains poorly investigated.
BCS significantly reduces the risk from suicide among females with breast cancer.
The suicide rate after BCS is not higher than that of the general population.
BCS offers a compelling option for improving the self-esteem of patients with cancer.
Breast cancer is the most prevalent malignancy among females globally1, and the leading cause of cancer-related death in females. According to the Global Cancer Statistics 2020 report by the International Agency for Research on Cancer, breast cancer has surpassed lung cancer as the most commonly diagnosed cancer in females2.
Surgery, including breast-conserving surgery (BCS) and mastectomy, is the primary treatment for breast cancer. The emergence of BCS dates back to the 1970s. Three major clinical trials3–5, conducted in different countries, demonstrated that both BCS and mastectomy exhibited comparable overall survival and local recurrence rates and provided evidence supporting the viability and safety of BCS. A recent study demonstrated the long-term oncological safety of BCS in centrally located breast cancer compared with mastectomy6. Based on these studies, BCS has changed the understanding of the biology of breast cancer, thus advancing the use of BCS in early breast cancer. Since the 1980s, BCS has quickly replaced total mastectomy as the treatment of choice for early-stage breast cancer in Europe and the US. In the US, 65.9% of women patients with breast cancer underwent BCS between 1995 and 20087, and a 2010 study of early-stage breast cancer data from four European countries showed 78% of patients underwent BCS8. However, in developing countries, such as the Arab countries, a 2006 study showed that 80% of female patients with breast cancers still underwent total mastectomy9. In China, the rate of BCS is distributed unevenly; in South China, the rate of BCS is 47.1%, while in Northeast China, it is only 8.9%10. Thus, there exists difference in the rate of BCS between developed and developing countries, and greater awareness and application of BCS is needed in developing countries.
In 2020, suicide was ranked as the 12th leading cause of death in all age groups in the US11. Compared with the general population, patients with cancer experience significantly higher suicide-related mortality, while female patients with any cancer had a higher suicide rate than the general female population [standardized mortality ratio (SMR) 1.59 (95% CI 1.27–1.97)]12. Therefore, it is essential to further examine the mental health of cancer survivors. BCS is recommended for females with early-stage breast cancer because its oncological outcomes are equivalent to that of mastectomy13. Additionally, BCS has been shown to improve body image, future perspectives, and, hence, quality of life and self-esteem in patients with breast cancer compared with mastectomy14. Thus, we hypothesized that patients who underwent BCS may have a lower risk for suicide, which can reflect the impaired socioeconomic status and high rates of depression among cancer patients15. Therefore, we aimed to compare the suicide risk between female patients with breast cancer who underwent BCS and those who underwent mastectomy.
Subjects and methods
Data source and study population
A retrospective cohort study was conducted to test the hypothesis using data from the National Cancer Institute’s Surveillance, Epidemiology, and End Results (SEER) Program, a population-based cancer registry that provides comprehensive information regarding age at diagnosis, sex, race, year of diagnosis, cancer demographics, anatomical site, histology, stage, therapy, socioeconomic status, and vital statistics of ~30% of individuals with cancer in the US16. In addition, data from the SEER program enable comparisons with the general population, making it possible to estimate cancer mortality and survival17.
Patients with first primary breast cancer, newly diagnosed between 2000 and 2020, were identified from the SEER 18 database (2022 edition) using SEER*Stat software. Patients with diagnoses based solely on death certificates or autopsies were excluded. Additionally, participants with incomplete information regarding age at diagnosis, race, or follow-up were also excluded. For comparison, age-specific, race-specific, and year-specific mortality data for the US general population between 2000 and 2020 were extracted from the National Center for Health Statistics using SEER*Stat software. This study was performed according to the STROCSS 2021 guideline18, Supplemental Digital Content 1, http://links.lww.com/JS9/B681.
Study variables
For all patients, the follow-up period commenced at the time of breast cancer detection and concluded at the time of death from any cause, or at the end of the research period (31 December 2020). Data regarding patient demographics and clinical information from the SEER database, including age, race, year of diagnosis, residential area, median house-hold income, stage, follow-up time, surgical modality, and cause of death, were collected. Patients with “Suicide and Self-Inflicted Injury (50220)” recorded as the cause of death were presumed to have committed suicide. Age was categorized into four groups: 18–39, 40–59, 60–79, and older than or equal to 80 years of age. Race was categorized as white, black, American Indian/Alaskan Native (AI/AN), and Asian or Pacific Islanders (API). Years of diagnosis were categorized into four periods: 2000–2004, 2005–2009, 2010–2014, and 2015–2020. Median house-hold income was categorized into four groups: low (< $35 000); median ($35 000 to $75 000); high (> $75 000); and unknown. Surgery types were categorized into three groups according to the surgery coding and staging manual of the SEER program: BCS; total/radical mastectomy; and no surgery.
Statistical analysis
The suicide rate among patients with breast cancer was determined by calculating the reported suicide rate per 100 000 person-years of follow-up. Mortality and SMR from suicide were calculated in accordance with a previous study19. SMR represents the risk for death from suicide compared with the matched cancer-free population with a similar distribution of age at diagnosis, race, and year of diagnosis in the US population during the same period. SMR was estimated as the ratio of the observed to the expected number of deaths. Observed deaths represent the total number of deaths from suicide among patients with cancer recorded during the study period, whereas expected deaths represent the number of individuals who died of suicide in the general population, with a similar distribution of age at diagnosis, race, and calendar year. Cumulative mortality rate (CMR) was calculated to identify breast cancer survivors at higher risk for death. Multivariate Cox regression analysis was performed to compare the mortality risk within subgroups of patients with cancer. Differences with P less than 0.05 were considered to be statistically significant. Analyses were performed using SEER*Stat software and R statistical software (R Foundation for Statistical Computing).
Results
Patient characteristics
A total of 1 190 991 patients, from 2000 to 2020, were extracted from the SEER database (Fig. 1 and Table 1), with a median follow-up of 6.8 years (range, 0–20.9 years) and a total follow-up of 9 412 140 years. Among these patients, 62 168 (5.2%) were 18–39, 523 121 (43.9%) were 40–59, 503 267 (42.3%) were 60–79, and 102 435 (8.6%) were older than 80 years of age. In terms of race, most patients were white, accounting for 949 132 (79.7%) of the total, followed by 124 631 (10.5%) black, 110 221 (9.3%) API, and 7007 (0.6%) AI/AN patients. The number of breast cancer diagnoses increased annually, with 372 223 (31.3%) patients diagnosed between 2015 and 2020, 290 635 (24.4%) between 2010 and 2014; 270 146 (22.7%) between 2005 and 2009; and 257 987 (21.7%) between 2000 and 2004. Regarding median house-hold income, most patients with breast cancer had a median or high income (99.3%), while a small percentage had a low income (0.7%). Similarly, most patients with breast cancer resided in urban areas, with only 10.5% residing in rural areas. In terms of cancer stage, more than one-third of breast cancer patients were classified as localized, 18.3% as regional, 13.8% as in situ, and 3.9% as distant. Regarding surgery, 56.5% of the patients underwent BCS, 36.1% underwent total/radical mastectomy, and 7.4% did not undergo surgery. In terms of PR status, 62.2% of breast cancers had positive status, 25.0% were negative, and 12.9% were unknown. Regarding HR/HER2 subtype, 31.9% of patients with breast cancer were HR+/HER2−, 4.8% were HR+/HER2+, 4.7% were HR−/HER2−, 2.0% were HR+/HER2−, and 56.5% were unknown. In terms of chemotherapy, 33.7% of patients with breast cancer received chemotherapy and the rest did not receive it. Regarding radiotherapy, 49.3% of patients with breast cancer received it and 50.7% did not receive it (Table 1).
Figure 1.
Inclusion and exclusion criteria of females with breast cancer in this study.
Table 1.
Demographic and clinical characteristics of women with breast cancer in the SEER 18 registries from 2000 to 2020.
| Characteristics | No. patients, n (%) | Follow-up time in total (years) |
|---|---|---|
| All patients | 1,190,991 (100.0) | 9,412,140 |
| Age | ||
| 18–39 | 62,168 (5.2) | 514,851 |
| 40–59 | 523,121 (43.9) | 4,652,135 |
| 60–79 | 503,267 (42.3) | 3,733,411 |
| 80+ | 102,435 (8.6) | 511,742 |
| Race | ||
| White | 949,132 (79.7) | 7,659,782 |
| Black | 124,631 (10.5) | 871,447 |
| AI/AN | 7,007 (0.6) | 51,341 |
| API | 110,221 (9.3) | 829,570 |
| Year of diagnosis | ||
| 2000–2004 | 257,987 (21.7) | 3,433,994 |
| 2005–2009 | 270,146 (22.7) | 2,879,677 |
| 2010–2014 | 290,635 (24.4) | 2,091,403 |
| 2015–2020 | 372,223 (31.3) | 1,007,066 |
| Median house-hold incomea | ||
| Low | 8,082 (0.7) | 53,535 |
| Median | 642,168 (53.9) | 5,054,970 |
| High | 540,505 (45.4) | 4,302,039 |
| Unknown | 236 (0.0) | 1,595 |
| Rural/urban status | ||
| Rural | 124,580 (10.5) | 979,159 |
| Urban | 1,064,803 (89.4) | 8,420,270 |
| Unknown | 1,608 (0.1) | 12,711 |
| Stage | ||
| In situ | 163,851 (13.8) | 1,839,600 |
| Localized | 441,207 (37.0) | 4,557,765 |
| Regional | 218,527 (18.3) | 2,050,796 |
| Distant | 46,129 (3.9) | 181,685 |
| Unstaged | 321,277 (27.0) | 782,294 |
| PR status | ||
| Negative | 297,525 (25.0) | 2,207,683 |
| Positive | 740,415 (62.2) | 5,595,625 |
| Unknown | 153,051 (12.9) | 1,608,832 |
| HR/HER2 subtype | ||
| HR+/HER2+ | 57,614 (4.8) | 267,006 |
| HR+/HER2− | 379,569 (31.9) | 1,760,731 |
| HR−/HER2+ | 24,175 (2.0) | 108,877 |
| HR−/HER2− | 56,296 (4.7) | 236,048 |
| Unknown | 673,337 (56.5) | 7,039,477 |
| Surgery | ||
| Breast-conserving surgery | 672,676 (56.5) | 5,658,017 |
| Total/radical mastectomy | 429,717 (36.1) | 3,419,786 |
| No surgery | 88,598 (7.4) | 334,337 |
| Chemotherapy | ||
| Yes | 401,332 (33.7) | 3,186,739 |
| No/Unknown | 789,659 (66.3) | 6,225,401 |
| Radiotherapy | ||
| Yes | 587,090 (49.3) | 4,806,331 |
| No/Unknown | 603,901 (50.7) | 4,605,808 |
AI/AN, American Indian/Alaska Native; API, Asian or Pacific Islander; HER2, human epidermal growth factor receptor 2; HR, hormone receptor; PR, progesterone receptor; SEER, Surveillance, Epidemiology, and End Results; SMR, standardized mortality ratio.
Low house-hold income represents those with a house-hold income less than $35,000, while median house-hold income represents those with a house-hold income between $35,000 and $75,000, and high house-hold income represents those with a house-hold income more than $75,000.
Incidence of suicide among female breast cancer survivors
In this cohort, there were 667 recorded deaths from suicide, with a mortality rate of 7.09 per 100 000 person-years, which was significantly higher than that of the matched general population [SMR 1.06 (95% CI 0.98–1.14)]. Specifically, patients who underwent mastectomy exhibited significantly higher suicide mortality than the general population [mortality rate, 8.16 per 100 000 person-years; SMR 1.18 (95% CI 1.05–1.33)], while there was no significant difference in suicide rate between patients who underwent BCS and the general population [SMR 0.92 (95% CI 0.83–1.02)] (Table 2).
Table 2.
The mortality from suicide in women with breast cancer, compared with general population using SMR.
| Cancer population | General population | ||||
|---|---|---|---|---|---|
| Characteristics | No. observed deathsa, n (%) | Mortality rateb | No. expected deathsa (%) | Mortality rateb | SMRc (95% CI) |
| All patients | 667 (100) | 7.09 | 630.8 | 6.70 | 1.06 (0.98–1.14) |
| Surgery | |||||
| Breast-conserving surgery | 343 (51.4) | 6.06 | 372.8 | 6.59 | 0.92 (0.83–1.02) |
| Total/radical mastectomy | 279 (41.8) | 8.16 | 236.4 | 6.91 | 1.18 (1.05–1.33) |
| No surgery | 45 (6.8) | 13.46 | 21.6 | 6.47 | 2.08 (1.55–2.78) |
| Age | |||||
| 18–39 | 46 (6.9) | 8.93 | 30.9 | 6.00 | 1.49 (1.12–1.99) |
| 40–59 | 399 (59.8) | 8.58 | 382.6 | 8.22 | 1.04 (0.95–1.15) |
| 60–79 | 199 (29.8) | 5.33 | 195.6 | 5.24 | 1.02 (0.89–1.17) |
| 80+ | 23 (3.5) | 4.49 | 21.8 | 4.26 | 1.06 (0.70–1.59) |
| Race | |||||
| White | 599 (89.8) | 7.82 | 575.1 | 7.51 | 1.04 (0.96–1.13) |
| Black | 16 (2.4) | 1.84 | 18.4 | 2.11 | 0.87 (0.53–1.42) |
| AI/AN | 5 (0.8) | 9.74 | 1.9 | 3.75 | 2.60 (1.08–6.24) |
| API | 47 (7.0) | 5.67 | 35.4 | 4.27 | 1.33 (1.00–1.77) |
| Year of diagnosis | |||||
| 2000–2004 | 199 (29.8) | 5.80 | 205.7 | 5.99 | 0.97 (0.84–1.11) |
| 2005–2009 | 212 (31.8) | 7.36 | 192.0 | 6.67 | 1.10 (0.97–1.26) |
| 2010–2014 | 167 (25.0) | 7.99 | 155.3 | 7.42 | 1.08 (0.92–1.25) |
| 2015–2020 | 89 (13.4) | 8.84 | 77.9 | 7.73 | 1.14 (0.93–1.41) |
| Median house-hold incomed | |||||
| Low | 3 (0.5) | 5.60 | 3.8 | 7.01 | 0.80 (0.26–2.48) |
| Median | 361 (54.1) | 7.14 | 336.1 | 6.65 | 1.07 (0.97–1.19) |
| High | 303 (45.4) | 7.04 | 290.9 | 6.76 | 1.04 (0.93–1.17) |
| Unknown | 0 | 0.00 | 0.1 | 7.14 | 0.00 (0.00–NA) |
| Rural/urban status | |||||
| Rural | 63 (9.4) | 6.43 | 66.2 | 6.77 | 0.95 (0.74–1.22) |
| Urban | 602 (90.3) | 7.15 | 564.0 | 6.70 | 1.07 (0.99–1.16) |
| Unknown | 2 (0.3) | 15.73 | 0.6 | 4.34 | 3.63 (0.91–14.50) |
| Stage | |||||
| In situ | 107 (16.1) | 5.82 | 124.3 | 6.75 | 0.86 (0.71–1.04) |
| Localized | 293 (43.9) | 6.43 | 295.6 | 6.49 | 0.99 (0.88–1.11) |
| Regional | 176 (26.4) | 8.58 | 139.5 | 6.80 | 1.26 (1.09–1.46) |
| Distant | 19 (2.8) | 10.46 | 12.3 | 6.79 | 1.54 (0.98–2.42) |
| Unstaged | 72 (10.8) | 9.20 | 59.1 | 7.56 | 1.22 (0.97–1.53) |
| PR status | |||||
| Negative | 155 (23.3) | 7.02 | 143.0 | 6.48 | 1.08 (0.93–1.27) |
| Positive | 399 (59.8) | 7.13 | 384.7 | 6.88 | 1.04 (0.94–1.14) |
| Unknown | 113 (16.9) | 7.02 | 103.2 | 6.41 | 1.10 (0.91–1.32) |
| HR/HER2 subtype | |||||
| HR+/HER2+ | 17 (2.5) | 6.37 | 20.8 | 7.78 | 0.82 (0.51–1.32) |
| HR+/HER2− | 137 (20.5) | 7.78 | 132.4 | 7.52 | 1.03 (0.88–1.22) |
| HR−/HER2+ | 15 (2.3) | 13.78 | 8.2 | 7.49 | 1.84 (1.11–3.05) |
| HR−/HER2− | 30 (4.5) | 12.71 | 16.8 | 7.11 | 1.79 (1.25–2.56) |
| Unknown | 468 (70.2) | 6.65 | 452.8 | 6.43 | 1.03 (0.94–1.13) |
| Chemotherapy | |||||
| Yes | 254 (38.1) | 7.97 | 228.0 | 7.15 | 1.11 (0.99–1.26) |
| No/Unknown | 413 (61.9) | 6.63 | 402.9 | 6.47 | 1.03 (0.93–1.13) |
| Radiotherapy | |||||
| Yes | 259 (38.8) | 5.39 | 324.3 | 6.75 | 0.80 (0.71–0.90) |
| No/Unknown | 408 (61.2) | 8.89 | 306.6 | 6.66 | 1.33 (1.21–1.47) |
AI/AN, American Indian/Alaska Native; API, Asian or Pacific Islander; HER2, human epidermal growth factor receptor 2; HR, hormone receptor; PR, progesterone receptor; SMR, standardized mortality ratio.
Observed deaths represent the total number of deaths from fatal infections among patients with cancer recorded during the study period. Expected deaths represent the number of individuals who died of fatal infections in the general population with a similar distribution of age at diagnosis, sex, race, and calendar year.
Mortality rate was represented as per 100 000 person-years.
The SMRs were estimated as the ratios of observed to expected number of deaths. The observed values represented the number of deaths in cancer patients, whereas the expected values represented the number of individuals who died of the same causes in the general population, with a similar distribution of age, sex, race, and calendar year.
Median house-hold income was categorized into four groups: low (< $35 000); median ($35 000 to $75 000); high (> $75 000); and unknown.
In terms of age group, there were 46,399,199 and 23 suicide cases in the 18–39, 40–59, 60–79, and older than 80 years groups, respectively. The mortality rate was higher in the younger age group (18–39 years) compared with that in the other age groups in the cancer population. When compared with the general population, patients in the 18–39 years group had significantly higher suicide mortality [mortality rate, 8.93 per 100 000 person-years; SMR 1.49 (95% CI 1.12–1.99)]. Among the races, white patients exhibited a higher rate of suicide (7.82 per 100 000 person-years), and a higher risk for suicide compared with the general white population [SMR 1.04 (95% CI 0.96–1.13)]. AI/AN breast cancer survivors exhibited the highest risk for suicide compared to the general population [mortality rate, 9.74 per 100 000 person-years; SMR 2.60 (95% CI 1.08–6.24)]. A gradually increased incidence rate of suicide and SMRs was observed from survivors diagnosed from 2000 to 2004 [mortality rate, 5.80 per 100 000 person-years; SMR 0.97 (95% CI 0.84–1.11)] compared with those diagnosed from 2015 to 2020 [mortality rate, 8.84 per 100 000 person-years; SMR 1.14 (95% CI 0.93–1.41)]. A significantly higher suicide rate was observed in those with a median house-hold income [mortality rate, 7.36 per 100 000 person-years; SMR 1.07 (95% CI 0.97–1.19)], or a high house-hold income [mortality rate, 7.99 per 100 000 person-years; SMR 1.04 (95% CI 0.93–1.17)], while the suicide mortality rate between breast cancer patients who had low house-hold income and the general population exhibited no significant difference. Patients with breast cancer residing in urban areas exhibited a higher suicide mortality rate than the general population, whereas no significant difference was observed among those residing in rural areas. Moreover, the suicide mortality rate for survivors of regional breast cancer was higher than that of the general population [mortality rate, 8.58 per 100 000 person-years; SMR 1.26 (95% CI 1.09–1.46)]. Distant breast cancer survivors exhibited the highest risk for suicide compared to the general population [mortality rate, 10.46 per 100 000 person-years; SMR 1.54 (95% CI 0.98–2.42)]. In addition, patients with HR-/HER2- had higher suicide mortality than the general population [mortality rate, 12.71 per 100 000 person-years; SMR 1.79 (95% CI 1.25–2.56)], while patients with HR−/HER2+ had higher suicide mortality than the general population [mortality rate, 13.78 per 100 000 person-years; SMR 1.84 (95% CI 1.11–3.05)]. As for chemotherapy, no significant difference was observed among those breast cancer survivors. A significantly higher suicide rate was observed in those treated without radiotherapy or unknown [mortality rate, 8.89 per 100 000 person-years; SMR 1.33 (95% CI 1.21–1.47)] (Table 2).
Mortality risk factors for suicide among breast cancer survivors
The cumulative suicide mortality rate was analyzed to determine the subgroup with the greatest risk for death among breast cancer survivors who underwent surgery. The long-term cumulative suicide mortality rate was significantly lower in patients who underwent BCS than in those who underwent mastectomy (10-year cumulative mortality rate, 0.059% versus 0.083%, respectively; P = 0.0003) (Fig. 2).
Figure 2.
Cumulative mortality rate of suicide among women with breast cancer in the Surveillance, Epidemiology and End Results 18 registries, comparing breast-conserving surgery and mastectomy.
In multivariate Cox analyses, when compared with mastectomy, BCS was associated with a significantly decreased risk of suicide among females with breast cancer [hazard ratio (HR) 0.80 (95% CI 0.68–0.95); P = 0.009], while no surgical intervention was associated with significantly increased risk from suicide [HR 1.64 (95% CI 1.17–2.29); P = 0.004] (Table 3).
Table 3.
Multivariable Cox analysis for suicide rate among subgroups of patients with breast cancer.
| Variable | HR (95% CI) | p |
|---|---|---|
| Surgery | ||
| Breast-conserving surgery | 0.80 (0.68–0.95) | 0.009 |
| Total/radical mastectomy | Reference | |
| No surgery | 1.64 (1.17–2.29) | 0.004 |
| Age | ||
| 18–39 | Reference | |
| 40–59 | 0.99 (0.73–1.35) | 0.9 |
| 60–79 | 0.59 (0.42–0.82) | 0.002 |
| 80+ | 0.43 (0.26–0.72) | 0.001 |
| Race | ||
| White | 1.15 (0.37–3.59) | 0.8 |
| Black | 0.24 (0.07–0.83) | 0.02 |
| API | 0.77 (0.24–2.46) | 0.6 |
| AI/AN | Reference | |
| Year of diagnosis | ||
| 2000–2004 | Reference | |
| 2005–2009 | 1.31 (1.07–1.61) | 0.01 |
| 2010–2014 | 1.44 (1.03–2.01) | 0.03 |
| 2015–2020 | 1.47 (0.92–2.34) | 0.1 |
| Median house-hold incomea | ||
| Low | 0.83 (0.26–2.66) | 0.7 |
| Median | 1.04 (0.88–1.22) | 0.6 |
| High | Reference | |
| Unknown | 1.0 | |
| Rural/urban status | ||
| Rural | Reference | |
| Urban | 1.13 (0.86–1.49) | 0.4 |
| Unknown | 2.81 (0.46–17.14) | 0.3 |
| Stage | ||
| In situ | 0.68 (0.40–1.18) | 0.2 |
| Localized | 0.87 (0.53–1.43) | 0.6 |
| Regional | 1.10 (0.67–1.81) | 0.7 |
| Distant | Reference | |
| Unstaged | 0.93 (0.51–1.70) | 0.8 |
| PR status | ||
| Negative | Reference | |
| Positive | 1.14 (0.92–1.42) | 0.2 |
| Unknown | 1.31 (0.99–1.74) | 0.06 |
| HR/HER2 subtype | ||
| HR+/HER2− | Reference | |
| HR−/HER2− | 1.93 (1.24–3.02) | 0.004 |
| HR−/HER2+ | 1.87 (1.05–3.30) | 0.032 |
| HR+/HER2+ | 0.78 (0.47–1.30) | 0.3 |
| Unknown | 1.11 (0.79–1.55) | 0.5 |
| Chemotherapy | ||
| Yes | 0.89 (0.73–1.09) | 0.3 |
| No/Unknown | Reference | |
AI/AN, American Indian/Alaska Native; API, Asian or Pacific Islander; HER2, human epidermal growth factor receptor 2; HR, hazard ratio; HR, hormone receptor; PR, progesterone receptor.
Bold values represent the statistically significant results.
Median house-hold income was categorized into four groups: low (< $35 000); median ($35 000 to $75 000); high (> $75 000); and unknown.
Multivariate Cox analysis further revealed that survivors between 60 and 79 years of age [vs. 18–39 years: HR 0.57 (95% CI 0.42–0.82); P = 0.002], older than 80 years [vs. 18–39 years: HR 0.43 (95% CI 0.26–0.72); P = 0.001], or black race [vs. AN/AI: HR 0.24 (95% CI 0.07–0.83); P = 0.02] were associated with significantly decreased risk for suicide, and HR−/HER2− [vs. HR+/HER2−: HR 1.93 (95% CI 1.24–3.02); P = 0.004], HR−/HER2+ [vs. HR+/HER2−: HR 1.87 (95% CI 1.05–3.30); P = 0.032] were associated with significantly increased risk for suicide. The result revealed that the year of diagnosis was not a statistically significant risk factor for suicide among breast cancer survivors. In addition, house-hold income [low vs. high: HR 0.83 (95% CI 0.26–2.66); P = 0.7; median vs. high; HR 1.04 (95% CI 0.88–1.22); P = 0.6], residence [urban vs. rural: HR 1.13; (95% CI 0.86–1.49); P = 0.4], tumour stage [in situ vs. distant: HR 0.68 (95% CI 0.40–1.18); P = 0.2; localized vs. distant: HR 1.87 (95% CI 0.53–1.43); P = 0.6; regional vs. distant: HR 1.10 (95% CI 0.51–1.70); P = 0.7], PR status [positive vs. negative: HR 1.14; (95% CI 0.92–1.42); P = 0.3], and chemotherapy [yes vs. no/unknown: HR 0.89; (95% CI 0.73–1.09); P = 0.3] did not exhibit any statistically significant difference among patients with breast cancer (Table 3).
Mortality risk of suicide in patients with breast cancer according to surgical intervention(s) across different age groups
An elevated risk for suicide was observed in younger patients with breast cancer (Table 3), indicating that the burden of breast cancer was more pronounced in younger age groups.
Subsequently, we investigated whether BCS could mitigate the risk of suicidal mortality in younger patients (Fig. 3). Compared with mastectomy, BCS was associated with significantly lower mortality from suicide in patients younger than 65 years of age (P = 0.006) (Fig. 3A). In contrast, among individuals older than or equal to 65 years of age, BCS exhibited no such significant difference from mastectomy (P = 0.3) (Fig. 3B).
Figure 3.
Cumulative mortality rate of suicide among women with breast cancer in the Surveillance, Epidemiology and End Results 18 registries by age. (A) Cumulative mortality rate of suicide among women with breast cancer aged younger than 65 years, comparing breast-conserving surgery and mastectomy. (B) Cumulative mortality rate of suicide among women with breast cancer aged older than or equal to 65 years, comparing breast-conserving surgery and mastectomy.
Moreover, we explored whether BCS could impact the risk of suicide mortality in survivors who received chemotherapy or radiotherapy. The result revealed that BCS was associated with significantly lower suicide mortality in patients who did not receive radiotherapy or those with unknown status (P < 0.01) (Figure S1, Supplemental Digital Content 2, http://links.lww.com/JS9/B682), and exhibited no significant difference between those who did or did not receive chemotherapy (P = 0.4) (Figure S2, Supplemental Digital Content 2, http://links.lww.com/JS9/B682).
Discussion
Patients with cancer have a higher risk for suicide12; however, in this population-based study, including more than 1 million female patients with breast cancer, BCS was shown to be associated with significantly lower mortality from suicide than mastectomy, with a reduced mortality risk not higher than that of the general population.
The decreased mortality risk from suicide in those who underwent BCS reveals relief in burden and depression among female patients with breast cancer. A cancer diagnosis is an extremely impactful and life-changing event that often leads to significant psychological distress12. Numerous studies have reported that distress is common among cancer survivors, with 23–38% of patients diagnosed with cancer experiencing severe distress20–22. Depression, comorbidities, and pain are common risk factors for suicide23. In particular, pain is a pervasive symptom associated with cancer, as evidenced in a systematic review that found that 59% of patients undergoing anticancer treatment, 64% of those with advanced disease, and 33% after curative treatment reported pain24. The National Comprehensive Cancer Network Clinical Practice Guidelines in Oncology emphasized the importance of pain management in cancer treatment because it significantly affects the overall quality of life25. In addition, patients with cancer encounter numerous challenges and impairments related to their condition, including early retirement or unemployment, loss of independence, and instability in interpersonal relationships. These factors contribute to higher rates of depression and suicide among patients with cancer26.
A retrospective study had shown that depressive syndromes, especially major depression, were common clinical factors associated with suicide27. A nationwide cohort study showed that cancer patients with mental disorders were at higher suicide risk compared to those without28. Another Danish cohort study also showed that prostate cancer patients with previous depression had a three-fold increased risk for suicide compared with those without depression29, indicating that depression significantly elevated the risk of suicide death in cancer patients. A nationwide study revealed that depression rates in patients with breast cancer were higher than in the general inpatient population and compared to patients with no comorbidity, those with severe multimorbidity experienced an approximately three-fold increased depression among women with breast cancer [odds ratio 2.80, (95% CI 2.69–2.91)]30. According to previous studies, advanced stage30, fatigue and pain31, sociodemographic factors such as low education level, young age, and unemployment32 were found to be considerably associated with depression in breast cancer survivors. Furthermore, breast cancer patients who underwent mastectomy had higher levels of depression compared to those who underwent BCS32. As a result, it is necessary to evaluate the mental health of women with breast cancer. Exactly, a study suggested that patients with lung cancer and mental health disorder, participating in mental health treatment had a significant improvement in cancer mortality33. Behavioural interventions, such as meditation, yoga, and relaxation with imagery, are recommended for relieving depression in patients treated for breast cancer34.
The decreased mortality risk from suicide among females who undergo BCS may be due to the maintenance of quality of life and self-esteem. Breasts are recognized as a manifestation of secondary female sexual characteristics and are crucial to body image. Mastectomies often result in noticeable breast asymmetry, potentially leading to an altered perception of the patient’s appearance. Previous research has demonstrated a correlation between pronounced breast asymmetry and an increased likelihood of depressive symptoms35. Individuals undergoing surgical procedures face a multitude of physical, psychological, and social challenges that significantly affect their overall quality of life. BCS has emerged as a viable alternative for patients with breast cancer because advances in breast cancer surgery continue to evolve. The Danish randomized trial DBCG-82TM reported no significant disparity in the outcomes of 10-year recurrence-free survival (RFS) and 20-year overall survival (OS) between BCS and mastectomy36. Compared to mastectomy, BCS not only preserves the breast, but also minimizes trauma, facilitates speedier recovery, and sustains a positive body image. According to a Ghanaian study, most breast cancer survivors reported feeling unattractive due to the use of breast prostheses following mastectomy37. Sun and colleagues examined the psychological well-being of patients with breast cancer after BCS and modified radical resection in terms of quality of life. The study involved 50 patients undergoing BCS and 70 undergoing modified radical resection who were required to complete a self-report inventory at admission and six months after surgery, as well as self-rating depression scales on discharge and six months after surgery. These findings indicated that BCS had a lesser impact on the long-term psychological well-being of patients with breast cancer when compared with modified radical resection38.
Therefore, the results of the present study highlight the importance of improving the quality of life and self-esteem of female patients with breast cancer and provide a novel perspective on cancer management. In such settings, both breast reconstruction and BCS should be emphasized in clinical practice. The popularity of breast reconstruction has increased in recent years. A meta-analysis revealed that both breast reconstruction and BCS improved quality of life compared with total mastectomy, especially in terms of physical, social, and sexual health, including body image39. This suggests that breast reconstruction may be a more favourable option than total mastectomy for patients with breast cancer. However, breast reconstruction is not accessible to all patients, particularly those with local recurrence and distant metastases, because these are contraindications. Furthermore, the expense of breast reconstruction could be a significant barrier. One study revealed that breast cancer patients without health insurance had a lower likelihood of undergoing breast reconstruction than those who were privately insured40. The lack of financial support for breast reconstruction has led patients with breast cancer to opt for total mastectomy, an option that may potentially contribute to depression and suicide rates. Notably, postoperative complications may occur despite the execution of breast reconstruction41. In cases of unsuccessful initial reconstruction, patients may undergo a second breast reconstruction, placing additional physical and emotional burdens on them. These factors not only impact the physical well-being of patients but can also lead to psychological distress and despair. In breast cancer, the loss of positive body image resulting from mastectomy exacerbates the overall impact. Conversely, the preservation of body image through BCS can improve the quality of life, self-esteem, and future perspectives14; thus, it can serve as a protective factor against depression, which could further explain the lower incidence of suicide.
Our study revealed that patients treated with BCS and radiotherapy had a higher suicide rate. Radiotherapy is a main treatment for patients with breast cancer and is recommended for most patients with breast cancer after BCS. Radiotherapy does improve survival time in patients with cancer, but it may be associated with a lower quality of life, which may lead to suicide42.
NSABP trial demonstrated the clinical value of BCS combined with radiotherapy for early-stage breast cancer43. In 1990, the National Institutes of Health issued a consensus statement that BCS with radiotherapy was the preferred treatment for patients with unilateral breast cancer44, which promoted a significant increase in the proportion of BCS in developed countries. At present, BCS has become one of the standard surgery methods for early breast cancer. Breast conservation rates range from 50 to 70% in the United States45 and are close to 80% in Europe8. According to a previous study, the breast conservation rate is only 20.8% in China46, which may be related to the fact that most Chinese patients with breast cancer are younger and present with advanced cancer; therefore, BCS cannot be performed. In addition, developed countries recommend that early breast screening be carried out at an older age, while the age of incidence in patients with breast cancer in China is younger. Therefore, strengthening early screening is essential for BCS. Moreover, the doctor’s decision and cognition, as well as the patient’s choice, may also lead to the difference in the type of surgery10.
Based on the prevalence of depression in breast cancer patients, organizations or associations should pay attention to depression in breast cancer patients. Committee meetings should be held for breast cancer patients to put forward suggestions that benefit both their mental health and quality of life. It is essential for doctors and caregivers to offer patients, especially those after mastectomy, enhanced respect and care, so as to help patients feel the meaning of life, further aiding in the prevention of suicide.
Our study had several limitations, including a potential bias due to its retrospective design, limited detailed information on hormone therapy and immunotherapy, and lack of data regarding previous suicide attempts, psychiatric comorbidities such as anxiety and depression following cancer diagnosis. Moreover, our study did not assess the life satisfaction, quality of life, and depression status of breast cancer survivors. Nevertheless, this population-based study design provided a sufficient number of cases to investigate this relatively rare suicide event.
Conclusion
This retrospective cohort study, which included data from greater than 1 million females with breast cancer in the US, found that BCS was associated with an ~20% lower mortality risk from suicide than mastectomy. Suicide risk in patients who underwent BCS decreased to a level equivalent to that in the cancer-free population. Reduction in suicide risk from BCS represents a compelling example of improving the quality of life and self-esteem of patients with cancer and provides a novel perspective on cancer management.
Ethical approval
This study has been approved by the International Review Board of Sun Yat-sen University Cancer Center (SL-B2023-074-01).
Source of funding
This study was supported by National Key R&D Program of China [2021YFA1302100], Wu Jieping Medical Foundation (320.6750.2022-3-58), National Natural Science Foundation of China [32370698], Science and Technology Program of Guangzhou [202206080011] and Young Talents Program of Sun Yat-sen University Cancer Center [YTP-SYSUCC-0029].
Author contribution
H.L. and Z.X.L. had full access to all the data in the study and takes responsibility for the integrity of the data and accuracy of the data analysis. Y.Z., G.G., and J.L. contributed equally to this work as co-first authors. Y.Z.: data curation, investigation, writing—original draft, writing—review and editing. G.G.: methodology, investigation, writing—original draft, writing—review and editing. J.L.: formal analysis, investigation, writing—review and editing. Z.X.L.: data curation, investigation, supervision, validation, writing—review and editing. H.L.: supervision, validation, writing—review and editing.
Conflicts of interest disclosure
The author(s) have no potential conflicts of interest to disclose.
Research registration unique identifying number (UIN)
This study has been registered in Research Registry (ID: Researchregistry9554).
Guarantor
Dr. Lin had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.
Data availability statement
All data used in this study can be freely accessed from the SEER program (https://seer.cancer.gov/).
Supplementary Material
Acknowledgements
The interpretation and reporting of these data are the sole responsibility of the authors. The authors acknowledge the efforts of the National Cancer Institute and the Surveillance, Epidemiology, and End Results (SEER) Program tumour registries in the creation of the SEER database.
Footnotes
Sponsorships or competing interests that may be relevant to content are disclosed at the end of this article.
G.G., J.L. and Y.Z. contributed equally.
Supplemental Digital Content is available for this article. Direct URL citations are provided in the HTML and PDF versions of this article on the journal's website, www.lww.com/international-journal-of-surgery.
Published online 11 January 2024
Contributor Information
Guiping Guo, Email: 1113243681@qq.com.
Junteng Li, Email: lijt@sysucc.org.cn.
Yongqiang Zheng, Email: zhengyq@sysucc.org.cn.
Ze-Xian Liu, Email: liuzx@sysucc.org.cn.
Huan Lin, Email: linhuan2@gzucm.edu.cn.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
All data used in this study can be freely accessed from the SEER program (https://seer.cancer.gov/).