Current Practices toward Fertility Issues for Young Breast Cancer Patients: A Survey of the Korean Breast Cancer Society; The SMARTSHIP Study

Article information

J Breast Dis. 2020;8(2):100-107
Publication date (electronic) : 2020 December 31
doi : https://doi.org/10.14449/jbd.2020.8.2.100
1Department of Surgery, Catholic Kwandong University International St. Mary’s Hospital, Catholic Kwandong University College of Medicine, Incheon, Korea
2Institute of Biomedical Science, Catholic Kwandong University International St. Mary’s Hospital, Catholic Kwandong University College of Medicine, Incheon, Korea
3Department of Surgery, Chonbuk National University Hospital, Chonbuk National University College of Medicine, Jeonju, Korea
4Department of Surgery, Asan medical Center, University of Ulsan college of Medicine, Seoul, Korea
5Department of Surgery, Soonchunhyang Seoul Hospital, Soonchunhyang University College of Medicine, Seoul, Korea
6Breast Cancer Center, National Cancer Center, Goyang, Korea
Correspondence: Ilkyun Lee, M.D., PhD. Department of Surgery, Catholic Kwandong University International St. Mary’s Hospital, Catholic Kwandong University College of Medicine, 25 Simgok-ro 100 beon-gil, Seo-gu, Incheon 22711, Korea Tel: +82-32-290-3271, Fax: +82-32-290-3879 E-mail: iklee@ish.ac.kr, iklee68@gmail.com

The present research has been supported by Korea Breast Cancer Foundation.

Received 2019 September 5; Revised 2019 December 2; Accepted 2020 February 18.

Abstract

Purpose

This study aimed to investigate and analyze the current fertility-related practices for breast cancer patients; the results are intended to help improve the quality of life of young patients and survivors.

Methods

This study collected voluntary responses to a questionnaire that was used to survey Korean breast cancer specialists. The questionnaire consisted of five categories: knowledge, practice behaviors regarding fertility preservation, barriers to discussing fertility preservation, attitude toward fertility issues, and demographics and medical background.

Results

A total of 120 copies of the questionnaire were distributed; the response rate was 89%. The section of the questionnaire regarding knowledge indicated that most respondents had adequate fertility preservation knowledge for cancer patients. However, 13.1% of the respondents indicated that they thought pregnancy increased the cancer recurrence risk. Respondents’ knowledge and attitudes about fertility preservation were not correlated with actual practice. The absence of patient’s expressions (24.30%), high recurrence risk (27.10%), insufficient time in the clinic (21.50%), and hospital conditions such as no reproductive specialists or infertility clinic (16.82%), were considered major barriers to discussing fertility issues.

Conclusion

Although more than 50% of the respondents thought that cancer treatment is more important than fertility preservation and it is complex and difficult, the Korean breast surgical oncologists were generally encouraging when discussing fertility issues with young breast cancer patients. Hence, breast clinicians should share with young patients the updated evidence regarding the feasibility and safety of pregnancy after cancer treatment and the available options so that the best decisions can be made.

INTRODUCTION

With cancer prognosis improvement due to treatment development, quality of life has become an important problem for cancer survivors. Infertility in young cancer survivors, especially if they were childless at the time of cancer diagnosis, may impose significant psychological distress and impaired quality of life in areas of emotional well-being, sexuality, and relationship [1]. The infertility risk with cancer treatments widely varies and is dependent on the patient’s age as well as the treatment types and combinations received [2].

In Korea, over 90% of breast cancer patients survive more than 5 years after the primary treatment including surgery [3]. Moreover, the breast cancer incidence among Korean patients in their 40s is higher than that in Western countries where the proportion of premenopausal breast cancer patients is very low. The proportion of patients younger than 40 years with breast cancer in Korea is approximately 13%. It is nearly two times higher than that in Western countries [4]. Breast cancer patients under age 40 years can achieve successful pregnancy and childbirth after treatment for breast cancer. Moreover, it is known that pregnancy itself does not increase the risk of breast cancer recurrence [5,6].

Currently, many countries have conducted research regarding fertility preservation in young cancer patients, and patient referral systems [7-9]. In addition, fertility counseling and maintenance before cancer treatment in patients with childhood cancer have shown to improve the quality of life after cancer treatment [10].

The practice of oncologists regarding fertility preservation for cancer patients of reproductive age may depend on multiple factors, such as patient’s medical and psychosocial condition [11,12], patient’s knowledge [13], and physicians’ knowledge about fertility preservation [14].

However, at present, there are few studies on young breast cancer patients and survivors in Korea. Furthermore, most oncologists and patients tend to focus only on cancer treatment, and experience and knowledge of fertility preservation are not adequate. Particularly, young breast cancer patients and survivors’ pregnancy are unfamiliar subjects.

The purpose of this study was to investigate and analyze the current fertility-related practices for breast cancer patients, and the results are intended to help improve the quality of life of young breast cancer patients and survivors.

METHODS

This study was conducted as a questionnaire survey obtaining voluntary response from the Korean Breast Cancer Society (KBCS) members. The questionnaire used in this study was a modified form of the questionnaire used in Japanese studies, with permission obtained from the author [15]. The modified questionnaire was reconfirmed by the Korean Breast Cancer Survivor study group. The questionnaire consisted of 45 questions in five categories, namely, knowledge, practice behaviors regarding fertility preservation, barriers to discussing fertility preservation, attitude toward fertility issue, demographic and medical background (Table 1). The respondents were asked to self-evaluate their agreement with the statements using a fivegrade system (1. Strongly agree; 2. Agree; 3. Cannot decide; 4, Disagree; and 5. Strongly disagree). The questionnaire was distributed to the members of the Korean Breast Cancer Society who participated in the 2016 global breast cancer conference held at Jeju island. The questionnaire was distributed face-to-face and immediately collected after being answered. Approval for the study was obtained from our Institutional Review Board (IRB No. IS16QIS10054).

Questionnaire statements

Statistical analysis

Data regarding demographic and specialty factors were summarized as frequencies and percentages. The chi-square test was used for correlation analysis between physician knowledge, attitude, and background. The Fisher’s exact test was used when the frequency of each cell was less than 5. The odds ratios and their 95% confidence intervals were calculated using multivariate logistic regression analysis that examined the association between the fertility issues for young breast cancer patients and physician’s fertility preservation knowledge, attitude, age, sex, religion, duration, institute, number of staff, genetic clinic, and number of operation per month, partner, children, and death of a neighbor. Data analysis was performed using STATA (version 15.0 StataCorp LP College Station, TX, USA); p-values less than 0.05 were considered to represent a statistically significant difference.

RESULTS

A total of 120 copies of the questionnaire were distributed, of which 107 questionnaires were answered, resulting in a response rate of 89%. Respondent demographics and characteristics are listed in Table 2. Of the respondents, 40 (37.4%) were women, 97 (90.7%) were breast surgeons, 6 (5.6%) were medical oncologists, and 4 (3.7%) were other specialty physicians.

Demographic backgrounds (n=107)

Most respondents provided correct answers in the section regarding knowledge; the percentage of respondents who answered correctly ranged from 78% to 93%. However, 13.1% of the respondents indicated that pregnancy increased the recurrence risk, and 9.4% said they did not know if it increased cancer recurrence or not. Accuracy of knowledge about fertility was correlated with the number of staff where they worked (p=0.030). The affiliated institution (p=0.040) and the presence of a genetic counseling clinic (p=0.040) were significantly correlated with a positive opinion toward fertility preservation for breast cancer patients (Table 3).

Demographic factors associated with knowledge and attitude for fertility preservation

Respondents’ knowledge and attitudes about the fertility preservation were not correlated with actual practice. Further, patients brought up the fertility issue more voluntarily with physicians who worked at university hospitals, who worked at institutes with more staff (≥ 4), and who had a spouse. The discussion frequency with patients about infertility due to cancer treatments was lower for physicians who worked at hospitals that performed more monthly surgeries. The patient’s economic status was considered more by physicians who worked at hospitals with a large number of breast surgical oncologists. In case of patients with a high relapse risk, breast surgeons with more than 10 years of clinical experience are more likely to discuss fertility issue. Respondents without a relative or a friend who died and left a child behind and respondents who had more than a decade of experience with breast cancer treatment referred more patients to reproductive specialists. Moreover, respondents who were religious, worked at a hospital with a genetic clinic, and did not have a relative or a friend who died and left a child behind provided patients with more informative materials about fertility preservation (Table 4).

Factors associated with fertility-related practice behavior

The absence of patient’s interest in fertility (24.30%), high risk of breast cancer recurrence (27.10%), insufficient time in the clinic (21.50%), and hospital settings such as no reproductive specialists or infertility clinic (16.82%) were regarded as major obstacles for fertility issue discussion (Table 5).

Barriers for discussing fertility issues (n=107)

DISCUSSION

Recently published clinical practice guidelines by the American Society of Clinical Oncology and several other publications have highlighted fertility preservation and recommended offering fertility counseling to all young cancer patients before primary cancer treatment.

In the previous survey performed in Japan, almost one-third of the patients who expressed an interest in fertility selected a different adjuvant treatment than that treatment primarily recommended by the oncologist because of their desire to preserve fertility [16]. Therefore, young Korean breast cancer patients may choose a different adjuvant therapy if appropriate information regarding fertility preservation is provided before breast cancer treatment.

The practice of oncologists regarding fertility preservation for cancer patients of reproductive age may depend on multiple factors, such as patient’s medical and psychosocial condition [11,12], patient’s knowledge [13], and physicians’ fertility preservation experience [14]. This is the first study to describe the knowledge, attitudes, and behavior of breast surgical oncologists toward fertility issues in young Korean breast cancer patients. Although a previous survey in the United States showed that many breast cancer clinicians reported that they do not have knowledge of/or resources for fertility preservation [14], our results indicated that most respondents were well -aware of the current anti-cancer treatment impact on fertility and fertility preservation option such as oocyte cryopreservation, embryo cryopreservation, and ovarian tissue cryopreservation.

The present study showed that breast surgical oncologists generally had a positive attitude toward fertility preservation. The high response rate to this survey revealed the interest of KBCS members in fertility issue. A total of 89.7% (96/107) of the participants responded that they were positive in discussing fertility issue with young breast cancer patients. Although more than half of the respondents said that cancer treatment is more important than fertility preservation and that maintaining the ability to be pregnant is complicated and difficult, 40% of the respondents showed that they discussed issues related to childbearing with patients with high likelihood of relapse.

Results showed that 60% of the respondents always or often refer their patients to infertility specialists. This result was higher than in previous surveys performed in the United States (47%) and Japan (42%) [7,14]. However, these results indicate that 40% of breast surgical oncologists still do not refer patients to infertility specialists. The reason is not clear. However, 38% of the respondents answered that it is difficult for them to discuss fertility preservation because there are no fertility-related department or fertility experts at their hospitals.

Results of a study by Quinn et al. [6] showed that 47% of the responding oncologists often refer their patients to infertility specialists; however, these results indicate that more than half of the oncologists do not refer their patients. The likelihood of referring patients to infertility specialists was predicted by the sex and attitudes toward fertility preservation of oncologists. Female physicians are possibly more aware of patients’ desire for family and information regarding fertility-related issues. Velikova et al. [17] performed a qualitative study of quality of life issues and found that female oncologists were more willing to discuss sexuality and felt that such discussions had high impact on the survivors’ quality of life. However, there was no correlation in our study.

A high disease recurrence risk was considered the greatest barrier to discussing fertility for physicians, which was similar to the results of other studies [11,12]. When the patient had advanced breast cancer with a high likelihood of recurrence, both the patient and physician tended to refrain from discussing the future ability to achieve pregnancy. In this case, patient care should include not only referral to reproductive specialists but also informational, psychological, social, and religious (if applicable) support. Other reasons that were barriers to discussing fertility were patients not expressing an interest in fertility, insufficient medical consultation time, and hospital circumstances. Nevertheless, patients who did not voluntarily express an interest in fertility may have not known about the possibility of infertility due to cancer treatment or may have not known about fertility preservation. Therefore, if information had been provided about these issues, the results would have been different.

This study revealed that it is necessary to improve medical care by readjusting medical fees, increasing research regarding patient needs, and creating a system for patient referrals.

Forman et al. [18] showed that reluctance among physicians to discuss fertility preservation or to refer patients to fertility specialists is due to the associated costs. However, in our survey, only 6% of the respondents considered the patients’ economic circumstances. This seemed to be because most patients in Korea have private insurance that pays for their medical costs.

This study was limited by the small sample size and patients not being surveyed. Further investigations of patients’ needs are required because patients and physicians often have discordant perceptions of patients’ needs and problems. Another limitation of this study is that the results from the surveys may be biased due to the diverse roles of a breast surgical oncologist since each institution has their own different clinical practice, which may result in differences in the perceptions of fertility issues. This study will be meaningful as a study of the physician’s view of young breast cancer patients from the initial breast cancer diagnosis to further treatment plans.

In conclusion, although more than 50% of the respondents believed that cancer treatment is more important than fertility preservation and that fertility preservation is complex and difficult, Korean breast surgical oncologists were generally positive when discussing fertility issues with young breast cancer patients. Breast clinicians should share with young patients the updated evidence regarding the feasibility and safety of pregnancy after cancer treatment and the available options for fertility preservation so that the best decisions can be made.

Notes

The authors declare that they have no competing interests.

Acknowledgements

The authors sincerely thank the members of the Korean Breast Cancer Survivor study group (Study of Multi-disciplinARy Teamwork for breast cancer survivorSHIP: SMARTSHIP) who assisted the survey and the KBCS members who were willing to respond to the questionnaire. The present research has been supported by the Korea Breast Cancer Foundation.

References

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Article information Continued

Table 1.

Questionnaire statements

A. Knowledge about fertility issues of breast cancer patients
1. Total dose of alkylating agents are related to infertility
2. Pregnancy after breast cancer increases risk of recurrence
3. Pregnancy after chemotherapy increases risk of congenital anomaly
4. Pregnancy should be avoided during tamoxifen treatment
5. Luteinizing hormone releasing hormone (LHRH) analog reduces the risk of chemotherapy-induced amenorrhea
6. In the method of preserving the ability to be pregnant, what method do you know well?
B. Practice behavior
1. Patients voluntarily bring up the fertility issues in the clinic
2. I discuss the impact of cancer treatment to future fertility with my patients
3. I do not feel comfortable to discuss fertility issue with my patients
4. I take into account the history of childbirth when I discuss fertility issue with my patient
5. I take into account whether she has a spouse/partner when I discuss fertility issue with my patient
6. I take into account the economic status of the patient when I discuss fertility issue with my patient
7. I discuss fertility issues with breast cancer patients with high risk of recurrence
8. I refer patients who have questions about fertility to reproductive specialists
9. I provide my patients with educational material about fertility preservation
10. I use LHRH analog to preserve fertility reproductive specialists
C. Barriers for discussing fertility issues
1. The patient does not express their interest in fertility
2. The patient has high risk of recurrence
3. The patient has economic problems
4. The patient does not have a spouse/partner
5. There is no place/person to refer my patients to for fertility preservation
6. Time constraints affect my ability to discuss fertility preservation
7. What is the greatest difficulty in discussing fertility issues with young breast cancer patients?
D. Attitude toward fertility preservation
1. Patients with poor prognosis should not pursue fertility preservation
2. Treating cancer is more important than fertility preservation
3. Fertility preservation is difficult and complicated.
4. I fear passing hereditary cancer to a biological child
5. Losing mothers will negatively affect bereaved children
E. Demographics and medical backgrounds
1. What is your age?
2. What is your gender?
3. What is your religious background?
4. How long have you treated breast cancer patients?
5. What is your specialty?
6. What kind of institution do you practice in?
7. Where is your primary practice located?
8. How many breast surgeons are there in your practice setting including you?
9. Are there any female breast surgeon in your practice setting?
10. Are there any medical oncologists in your practice setting?
11. Are there any cancer-specialized pharmacists in your practice setting?
12. Is there a genetic counseling clinic in your practice setting?
13. In a month, how many breast cancer surgeries are performed in your practice setting?
14. In a month, how many breast cancer patients under 40 years of age do you see?
15. Do you have a spouse/partner?
16. Do you have children?
17. Do you have relatives or close friends who passed away leaving behind minor children?

Table 2.

Demographic backgrounds (n=107)

Characteristic No. (%)
Sex
 Male 67 (62.62)
 Female 40 (37.38)
Age (yr)
 30-39 38 (35.51)
 40-49 53 (49.53)
 50-59 12 (11.21)
 ≥ 60 4 (3.74)
Religion
 Protestant 44 (41.12)
 Catholic 27 (25.23)
 Buddhist 4 (3.74)
 Atheist 32 (29.91)
Career of breast cancer treatment (yr)
 <5 8 (7.48)
 5-10 26 (24.30)
 11-15 31 (28.97)
 16-20 30 (28.03)
 > 20 12 (11.21)
Specialty
 Breast surgeon 97 (90.65)
 Medical oncologist 6 (5.61)
 Others 4 (3.74)
Type of affiliation
 University hospital 83 (77.57)
 General hospital 18 (16.82)
 Special hospital 3 (2.80)
 Private clinic 3 (2.80)
Number of Breast surgeon
 1 11 (10.28)
 2-3 45 (42.06)
 4-5 21 (19.63)
 ≥6 30 (28.04)
Practice region
 Seoul 43 (40.19)
 Gyeonggi 20 (18.69)
 Gangwon 1 (0.93)
 Chungcheong 10 (9.35)
 Jeolla 17 (15.89)
 Gyeongsang 15 (14.02)
 Jeju 1 (0.93)
Female breast surgeon
 Present 73 (68.2)
 Absent 34 (31.8)
Medical oncologist
 Present 96 (89.72)
 Absent 11 (10.28)
Genetics clinic
 Present 57 (53.27)
 Absent 50 (46.73)
No. of breast cancer surgeries (per month)
 1-10 18 (16.82)
 11-50 58 (54.21)
 51-100 9 (8.41)
 > 100 22 (20.56)
No. of patients aged < 40 (per month)
 0-2 26 (24.30)
 3-5 38 (35.51)
 6-9 11 (10.28)
 ≥ 10 32 (29.90)
Partner/spouse
 Present 90 (84.11)
 Absent 17 (15.89)
Children
 Present 87 (81.31)
 Absent 20 (18.69)
Relatives/close friends who passed away leaving behind young children
 Present 29 (27.10)
 Absent 78 (72.90)

Table 3.

Demographic factors associated with knowledge and attitude for fertility preservation

Factor Knowledge
Attitude
No knowledge Knowledge p-value Unfavorable Favorable p-value
Age (yr)
 30-39 20 18 0.410* 12 26 0.310*
 40-49 19 34 15 38
 50-59 5 7 4 8
 ≥ 60 1 3 3 1
Gender
 Male 19 21 0.380 13 27 0.900
 Female 26 61 21 46
Religion
 Protestant 16 28 0.620* 10 34 0.120*
 Catholic 14 13 10 17
 Buddhist 2 2 0 4
 Atheist 13 19 14 18
Career of breast cancer treatment (yr)
 ≤5 6 2 0.310* 3 5 0.730*
 6-10 11 15 8 18
 11-15 14 17 11 20
 16-20 10 20 7 23
 > 20 4 8 5 7
Type of affiliation
 University hospital 32 51 0.470* 22 61 0.040*
 General hospital 10 8 10 8
 Special hospital 1 2 1 2
 Private clinic 2 1 1 2
Number of Breast surgeon
 1 5 6 0.030* 3 8 0.930*
 2-3 23 22 16 29
 4-5 11 10 6 15
 ≥6 6 24 9 21
Genetics clinic
 Present 22 35 0.440 23 34 0.040
 Absent 23 27 11 39
No. of breast cancer surgeries (per month)
 0-10 10 7 0.170* 5 12 0.890*
 11-20 13 17 8 22
 21-50 14 14 9 19
 51-100 3 6 4 5
 > 100 5 17 7 15
Partner/spouse
 Present 36 54 0.320 27 63 0.360
 Absent 9 8 7 10
Children
 Present 35 52 0.430 26 61 0.380
 Absent 10 10 8 12
Relatives/close friends who passed away leaving behind young children
 Present 16 13 0.090 11 18 0.400
 Absent 29 49 23 55
*

Fisher’s exact test.

Table 4.

Factors associated with fertility-related practice behavior

Variable OR (95% CI) p-value
B-1. Patients voluntarily bring up the fertility issues in the clinic Institute
University hospital 1.00
Others 0.21 (0.05-0.94) 0.040
No. of staff
1-3 1.00
≥4 17.82 (4.31-73.59) < 0.001
Partner
Yes 1.00
No 2.00e-10 (3.72e-11-1.07e-09) < 0.001
B-2. I discuss the impact of cancer treatment to future fertility with my patients No. of OP per month operation
≤ 10 1.00
11-100 0.12 (0.02-0.80) 0.030
> 100 0.05 (0.01-0.62) 0.020
B-6. I take into account the economic status of the patient when I discuss fertility issue with my patient No. of staff
1-3 1.00
≥4 3.34 (1.09-10.24) 0.030
B-7. I discuss fertility issues with breast cancer patients with high risk of recurrence Duration (yr)
≤ 10 1.00
11-20 4.96 (1.56-15.83) 0.010
> 20 12.19 0.070
B-8. I refer patients who have questions about fertility to reproductive specialists Duration (yr)
≤ 10 1.00
11-20 4.42 (1.29-15.18) 0.020
> 20 8.79 0.110
Death of a neighbor
Yes 1.00
No 4.23 (1.27-14.17) 0.020
B-9. I provide my patients with educational material about fertility preservation Religion
Yes 1.00
No 0.19 (0.06-0.60) 0.010
Gene clinic
Yes 1.00
No 0.32 (0.10-0.95) 0.040
Death of a neighbor
Yes 1.00
No 3.31 (1.05-10.48) 0.040

OR=odds ratio; CI=confidence interval; OP=operation.

Table 5.

Barriers for discussing fertility issues (n=107)

Variable No. (%)
The patient does not express their interest in fertility 26 (24.30)
The patient has high risk of recurrence 29 (27.10)
The patient has economic problems 7 (6.54)
The patient does not have a spouse/partner 4 (3.74)
There is no place/person to refer my patients to for fertility preservation 18 (16.82)
Time constraints affect my ability to discuss fertility preservation 23 (21.50)