Behavior, attitude, perception, and knowledge regarding fertility preservation among Chinese pediatric oncologists: a survey in China

Abstract

Purpose

Clinical specialists are supposed to inform childhood cancer patients of infertility risk and conduct fertility preservation (FP). However, little is known about whether doctors in China are fully prepared. This study aimed to investigate behavior, attitude, perception, and knowledge regarding FP among pediatric oncological specialists in a nation wide survey, to set the stage for improvements in current clinical practice patterns.

Methods

This study was conducted on physicians and surgeons specialized in pediatric oncology using a questionnaire through the WeChat platform. The behavior, attitude, perception, and knowledge were assessed by Likert questions and results were quantified to obtain scores. Data were then described and analyzed using R and GraphPad.

Results

Totally 373 specialists in pediatric tumors were included in the analysis. Hematologists, oncological surgeons, and reproductive medicine specialists won most trusts to be responsible for FP job. Most respondents did not have habits of delivering FP information or cooperating with FP specialists during treatment though they were well equipped with FP knowledge and desired for uniform national guideline for FP procedures. The severity of illness was regarded as the primary barrier of FP delivery. When a doctor was more educated and experienced, he was more likely to have better performance in FP. The total score, the knowledge score, and the single score concerning frequency of patients’ inquiry showed aggregational trend on geographic distribution.

Conclusion

Chinese pediatric oncologists demonstrated unsatisfactory practice behaviors based upon this self-reporting survey, although their attitude towards FP was generally positive.

Introduction

Approximately 17 out of every 100,000 people experience cancer in their childhood[1]. With an overall survival rate of cancer exceeding 80%[2], the focus of healthcare providers in cancer care is to help their patients manage with potential long‐term consequences of their treatment. A loss of fertility is a negative result of cancer treatment that adversely affects the quality of life of survivors. The St. Jude Lifetime Cohort Study recently showed that as many as 99.9% of childhood cancer survivors met the criteria of National Cancer Institute Common Terminology Criteria for Adverse Events-graded late effects on fertility as a result of their cancer or cancer-directed therapy, including gonadotoxicity-related potential for permanent azoospermia or premature ovarian insufficiency in survivors [3, 4].

The European Society of Medical Oncology[5], American Society of Clinical Oncology in the United States[6], American Society for Reproductive Medicine[7], and the Japan Society of Clinical Oncology[8, 9] encourage medical specialists to inform patients with cancer of the infertility risk and fertility preservation (FP) options before gonadotoxic treatments. However, in children, there is a physiologically hypogonadal period leading to a lack of exact measurement. Therefore, no reported data of fertility impairment in young children who are a major population of childhood cancer are available[10]. Many long-term follow-up studies on impaired reproductive ability in adult survivors of childhood cancer are required to show that FP is necessary in young patients[3, 4, 11]. The absence of a well-defined, strongly targeted guideline has resulted in conflicting knowledge on FP, low efficiency of referring patients with cancer to fertility specialists, and deficient communication between oncologists and fertility specialists[11, 12]. With the development of diagnostic and therapeutic technology, medical workers in China have witnessed great progress in childhood cancer survival approaching a world first-class level and an increased detectable rate of fertility impairment. Therefore, currently, China’s pediatric specialists are faced with the same challenge as counterparts in other countries regarding FP. This study aimed to investigate the behavior, attitude, perception, and knowledge regarding FP in Chinese medical workers who specialize in pediatric oncology nationwide.

Methods

Study design

The survey was designed in a plain text form based on a review of existing questionnaires regarding discussion of FP in medical professionals. An anonymous questionnaire was administered to the physician and surgeon members of China Anticancer Association who majored in pediatric oncology using the “Questionnaire Star” applet on the WeChat platform. Completion of the survey took approximately 10 min. Every member was limited to answer the questionnaire once. The questionnaire could only be submitted after all the questions were completed. Ethical approval for the study was obtained from the institutional Ethics Committee (SCMCIRB-K2022181-1). Eighteen directional choice questions were designed to demonstrate demographic information of the respondents. Nine questions were used to evaluate practice behaviors in FP clinical work on a 5-point Likert scale (never, seldom, sometimes, usually, and always, scored as 1–5). The scores of the nine questions were added up together to get the “behavior score.” The participants’ commitments to fulfill FP were assessed by oncologists’ agreement to six detailed types of barriers (yes, no, or not certain, which were scored as 1, 3, and 2, respectively), and the sum of those six questions was the “barrier score.” The attitudes were assessed by seven items, and each was scored from 1 to 5, representing agreement to the statement (from completely disagree to completely agree). The seven scores were piled up to get the “attitude score.” Six questions evaluated knowledge of FP (yes or no). Wrong answers were graded as 0 and correct answers were graded as 1 and then piled up together, so as to form a “knowledge score.” The “total score” was defined as the sum of the “behavior score,” the “barrier score,” the “attitude score,” and the “knowledge score.” The participants were also asked to choose the most primary barrier and the most appropriate department for being in charge of pediatric FP during treatment. Three more 5-point Likert scale questions were designed to evaluate medical professionals’ perception on how often patients’ parents would actively inquire about FP and how much the concern of the patient’s family regarding FP would be dependent on the economic status of the family or on the patient’s sex. The questionnaires are shown in detail in Supplementary Document 1.

Eligible study participants included Chinese physicians and surgeons who treated pediatric patients with cancer in all levels of Chinese hospitals in all provinces in China.

Statistical analysis

Analyses were conducted using R (version 4.2.1) and GraphPad. All P values were two sided, with a statistical significance level set at P < 0.05. Demographic data are shown as the number and percentage and these data were categorical variables in later regression analysis. A multiple linear regression model was used to determine the effect of variables on the “behavior score,” the “barrier score,” the “attitude score,” the “knowledge score,” and the “total score.” Other unordered multi-class variables in the questionnaire were included in a multinominal logistic regression model. Additionally, ordered multi-category variables were included in an ordinal multinomial logistic regression model. Variables were first compared in a single-factor regression model one by one, the ones with significant P values were then picked out in a multiple regression analysis. Odds ratios and their 95% confidence intervals were estimated. In order to facilitate multinominal logistic regression analysis, the respondents’ geographic distribution information was simplified and redivided into four geographical areas, the Northeast region, including Heilongjiang Province, Jilin Province, and Liaoning Province; the Eastern region, including Beijing, Tianjin, Shanghai, Hebei Province, Shandong Province, Jiangsu Province, Zhejiang Province, Fujian Province, Taiwan Province, Guangdong Province, Hong Kong Special Administrative Region, Macao Special Administrative Region, and Hainan Province; the Central region, including Shanxi Province, Henan Province, Hubei Province, Anhui Province, Hunan Province, and Jiangxi Province; and the Western region, including Inner Mongolia Autonomous Region, Xinjiang Uygur Autonomous Region, Ningxia Hui Autonomous Region, Shaanxi Province, Gansu Province, Qinghai Province, Chongqing City, Sichuan Province, Xizang Autonomous Region, Guangxi Zhuang Autonomous Region, Guizhou Province, and Yunnan Province. The spatial disparity of dependent variables was evaluated using Moran’s index.

Results

Demographic information of respondents

A total of 74.6% of the invited doctors returned the questionnaires. The study sample (n = 373) included 191 (51.2%) women. Hematologists (40.75%), physicians (20.64%), oncological surgeons (8.85%), and general surgeons (29.76%) from 28 provinces participated in the survey. Most of the respondents were highly experienced, with more than half of them having worked in cancer care for longer than 10 years. The marriage rate was 88%, and 84% of the respondents had one or more children. 78.02% of the participants had a Master degree or higher, and 32.71% of them had Doctor degree. 5.63% of the respondents had religious beliefs. Approximately 40% of the respondents worked in small departments with < 10 beds and < 5 colleagues. Over half of the respondents reported that no more than 100 patients each year were treated in the whole department. Most respondents were from Grade III level A teaching hospitals (3A represents the highest level of ability to provide medical care and medical education and conduct medical research in China; other levels are 3B, 2A, 2B, 1A, and 1B). However, only approximately half of the respondents claimed that their hospitals had the capability of radiotherapy or bone marrow transplantation. Demographic data are shown in detail in Table 1.

Table 1.

Basic information

Subjects		N (%)
Total		373 (100)
Sex	Male	182 (48.79)
	Female	191 (51.21)
Age (year)	20–30	31 (8.31)
	30–40	123 (32.98)
	40–50	131 (35.12)
	≥ 50	88 (23.59)
Education	Bachelor’s degree and below	82 (21.98)
	Master’s degree	169 (45.31)
	Doctoral degree	122 (32.71)
Specialization	Oncological surgeon	33 (8.85)
	General surgeon	111 (29.76)
	General physician	77 (20.64)
	Hematologist	152 (40.75)
Year of experience (year)	< 5	53 (14.21)
	5–10	75 (20.11)
	10–20	116 (31.1)
	≥ 20	129 (34.58)
Geographic position of hospital	Northeast China	54 (14.48)
	East China	227 (60.86)
	Central China	77 (20.64)
	West China	15 (4.02)
Level of hospital	3A	338 (90.62)
	3B and below	35 (9.38)
Teaching hospital	Yes	342 (91.69)
	No	31 (8.31)
Marriage	Single	36 (9.65)
	Married	329 (88.2)
	Divorced	8 (2.14)
Number of children	0	58 (15.55)
	1	224 (60.05)
	≥ 2	91 (24.4)
Religious belief	Yes	21 (5.63)
	No	352 (94.37)
Number of beds for cancer patients	≤ 10	165 (44.24)
	11–20	38 (10.19)
	21–50	80 (21.45)
	51–80	41 (10.99)
	≥ 81	49 (13.14)
Number of colleagues specialized in pediatric cancer in the same department	< 5	175 (46.92)
	5–10	81 (21.72)
	10–20	70 (18.77)
	> 20	48 (12.87)
Number of patients received per year	< 100	212 (56.84)
	100–300	76 (20.38)
	300–500	37 (9.92)
	> 500	48 (12.87)
Radiotherapy available in hospital	Yes	117 (31.37)
	No	256 (68.63)
Bone marrow transplantation available in hospital	Yes	236 (63.27)
	No	137 (36.73)
Reproductive medicine department in hospital	Yes	201 (53.89)
	No	172 (46.11)
Pediatric cancer patients in relatives	Yes	24 (6.43)
	No	349 (93.57)

Opinions in departments responsible for FP

A total of 3.49% of the physicians and 35.42% of the surgeons believed that pediatric surgeons should take charge of FP, while 57.64% of the physicians and 27.08% of the surgeons believed that hematologists should be mainly responsible. A total of 28.38% of the physicians and 28.47% of the surgeons preferred the “reproductive medicine specialist” to dominate FP during anticancer therapy. Hematologists and general physicians were prone to “hematologist” (OR = 3.5, 95%CI = 2.1 ~ 5.7, P = 8.1e − 7, OR = 3.7, 95%CI = 2.0 ~ 6.8, P = 1.8e − 5) rather than “surgeon” (OR = 0.075, 95%CI = 0.028 ~ 0.17, P = 9.5e − 9, OR = 0.18, 95%CI = 0.072 ~ 0.40, P = 8.5e − 5) being mainly responsible. Participants working in centers capable of doing radiotherapies showed more trust in hematologists on this question (OR = 1.6, 95%CI = 1.0 ~ 2.6, 0.042). Those who worked in medical centers with reproductive medicine departments preferred to choose “radiologist” (OR = 3.3, 95%CI = 1.2 ~ 12, P = 0.037), while those with marriage experience preferred not (OR = 0.28, 95%CI = 0.096 ~ 0.91, P = 0.022). Those who chose “completely agree” to the concept that “Parents of girls care more about FP” were less likely to trust reproductive experts in FP arrangement (OR = 0.33, 95%CI = 0.12 ~ 0.76, P = 0.016), but more likely to trust hematologists (OR = 2.1, 95%CI = 1.1 ~ 4.4, P = 0.032). Those who had higher behavior scores also gave less trust in reproductive experts (OR = 0.95, 95%CI = 0.92 ~ 0.99, P = 0.0096). Those who chose “severity of illness” as the most primary barrier in FP commitment tend to choosing “endocrinologist” in FP charging (OR = 4.4, 95%CI = 1.3 ~ 20, P = 0.027). Details are shown in Fig. 1A.

Fig. 1.

Forest plot; A relative factors regarding the choice of “who should predominate FP arrangement” (OR and 95%CI); B relative factors associated with the agreement of “Poor parents care less about FP” (OR and 95%CI); C relative factors regarding the agreement of “Parents of girls care more about FP” (OR and 95%CI); D relative factors on the choice of “Primary Barrier” (OR and 95%CI); E relative factors associated with “Barrier Score” (OR and 95%CI). OR, odd ratio; FP, fertility preservation; patients” sex: the perception that “Parents of girls care more about FP”; financial status: the perception that “Poor parents care less about FP”; active inquiry: the frequency that “Parents ask me about the impact of cancer treatment on their fertility”; Barrier 1: patients are too ill to get survival or to delay immediate treatment for FP; Barrier 2: patients cannot afford cost for FP; Barrier 3: parents are not willing to discuss FP; Barrier 4: there is no access to resort of FP; Barrier 5: heavy clinical work load causes lack of time to care about FP; Barrier 6: FP discussion may lead to treatment reluctance on malignancy

Perceptions of parents’ view of FP

When the respondents were asked about “whether the financial status would affect the willingness of parents to pursue FP for their children,” men were more likely to agree (OR = 1.6, 95%CI: 1.0–2.6, P = 0.039) or completely agree (OR = 2.9 95%CI: 1.2–7.4, P = 0.020) with the concept. Respondents with more experience also agreed more than those with < 5 years of experience (OR = 2.0, 95%CI = 1.1 ~ 3.8, P = 0.030). A higher barrier score which represented more commitment to FP execution was related with less agreement (“not sure” or more to “disagree” or less, OR = 0.88, 95%CI: 0.79–0.97, P = 0.0098; “agree” or more to “not sure” or less, OR = 0.84, 95%CI: 0.76–0.92, P = 0.00021; “completely agree” to “agree” or less, OR = 0.82, 95%CI: 0.69–0.96, P = 0.015). When the respondents were asked about the perception of “parents of female patients are more concerned about FP,” oncological surgeons were more positive than other specialists (OR = 4.6, 95%CI: 2.0–11, P = 0.00055). Participants who considered that “FP discussion may lead to treatment reluctance on malignancy” as the most primary barrier tended to agree more to this conception (OR = 3.8, 95%CI: 1.6–9.6, P = 0.016). The idea that hematologists should predominate FP arrangement also contributed to more agreement (OR = 5.3, 95%CI: 1.3–20, P = 0.0027). Working in a team of 5 or more colleagues (OR = 0.48, 95%CI: 0.30–0.76, P = 0.0022), with more than 20 beds (OR = 0.46, 95%CI: 0.25–0.83, P = 0.011) or in a center capable of bone marrow transplantation (OR = 0.21, 95%CI: 0.086–0.48, P = 0.00032), had negative correlation with agreement. Those with higher attitude scores tended to choose either “completely disagree” (OR = 1.3, 95%CI: 1.1–1.7, P = 0.041) or “agree” (OR = 1.1, 95%CI: 1.0–1.2, P = 0.0013) or even “completely agree” (OR = 1.3, 95%CI: 1.1–1.4, P = 0.00075) to this conception. We also found that agreement to those two questions had a positive correlation with each other (Fig. 1B and C).

Barrier evaluation

The primary barrier options for respondents were as follows: (1) patients are too ill to survive or to delay immediate treatment for FP; (2) patients cannot afford the cost of FP; (3) parents are not willing to discuss FP; (4) there is no access to performing FP; (5) a heavy clinical workload causes a lack of time to care about FP; (6) discussion on FP may lead to reluctance regarding treatment for malignancy. Selection of Barrier 1 (OR = 1.2, 95%CI: 1.1–1.3, P = 0.00014) and trust in endocrinologist in FP charging (OR = 6.2, 95%CI: 1.7–30, P = 0.0097) were associated with higher barrier score. Participants from Northeast China (OR = 0.90, 95%CI: 0.84–0.97, P = 0.0047) or with higher attitude scores (OR = 0.51, 95%CI: 0.26–0.97, P = 0.045) preferred not to choose Barrier 1. Higher attitude scores were also found associated with the selection of Barrier 4 (OR = 1.09, 95%CI: 1.02–1.17, P = 0.012). Those with higher behavior scores tended to blame Barrier 2 (OR = 1.06, 95%CI: 1.01–1.13, P = 0.027). Those aged over 50 years (OR = 3.3, 95%CI: 1.3–8.7, P = 0.014), or working in Western China (OR = 6.0, 95%CI: 1.2–22, P = 0.012) were more likely to choose Barrier 5. Those with Master or higher degree were unlikely to choose Barrier 3 (OR = 0.14, 95%CI: 0.060–0.40, P = 0.00013). Those having higher barrier scores were also unlikely to choose Barrier 3 (OR = 0.77, 95%CI: 0.64–0.91, P = 0.0034). Participants who likely chose Barrier 6 were those completely agreed with the statement that “parents of girls care more about FP” (OR = 5.2, 95%CI: 1.8–14, P = 0.0015), those who reported being consulted by patients about FP in an “always” frequency (OR = 27, 95%CI: 3.1–210, P = 0.0013), and those who had reproductive medicine department in their hospitals (OR = 5.8, 95%CI: 1.9–26, P = 0.0069). Details are shown in Fig. 1D. In general, men complained less about barriers than women (OR = 2.3, 95%CI: 1.4–3.8, P = 0.00066). Higher education level led to less complaint (OR = 1.9, 95%CI: 1.1–3.2, P = 0.022), while respondents from Northeast China tended to complain more (OR = 0.38, 95%CI: 0.19–0.77, P = 0.0073). Details are shown in Fig. 1E. Consent to Barrier 1 was only correlated to consent to Barrier 2 (OR = 1.6, 95%CI: 1.2–2.2, P = 0.0047), while consent to Barrier 6 was correlated to consent to all the Barriers except Barrier 1 (Barrier 2, OR = 1.6, 95%CI: 1.3–2.2, P = 0.00028; Barrier 3, OR = 1.7, 95%CI: 1.3–2.2, P = 0.00034; Barrier 4, OR = 1.7, 95%CI: 1.3–2.2, P = 4.2e − 5; Barrier 5, OR = 2.5, 95%CI: 1.9–3.3, P = 8.8e − 11).

Behavior evaluation

More than 80% of pediatric oncological practitioners rarely communicated with FP experts regarding treatments, even though 53.88% of the respondents knew the existence of Reproductive Medicine Department in their own hospitals. Less than 20% of the respondents volunteered to provide FP information and assistance to their patients, and only 15.55% would be consulted about FP by patients and their families in a “usually” or higher frequency. A total of 13% of the respondents reported that they had an established process regarding FP in their departments. Less than 10% of the respondents took measures or performed follow-up in FP treatment. Only 32.17% of the respondents were usually concerned of new developments in FP in their daily life.

The average behavior score was 23 ± 7, while the full score was 45, which represented a frequency of “seldom” to “sometimes” performing professional FP counseling. A doctoral degree educational background (OR = 10, 95%CI: 3.0–35, P = 0.00021), over 10 years of working experience (OR = 8.7, 95%CI: 2.7–27, P = 0.00030), and a better equipped hospital capable of radiotherapy (OR = 8.1, 95%CI: 2.5–26, P = 0.00059) all contributed to higher behavior scores. Those who reported a higher frequency receiving active consulting about FP tended to perform better in behavior scores (seldom to never, OR = 89, 95%CI: 8.2–960, P = 0.00025; sometimes to seldom, OR = 27, 95%CI: 8.2–89, P = 9.1e − 8). Consideration of “Patients cannot afford the cost of FP” as the primary barrier to FP was associated with higher behavior scores (OR = 31, 95%CI: 3.8–260, P = 0.0015). Regarding FP arrangement as the reproductive medicine specialists’ duty had a negative effect on the behavior score (OR = 0.25, 95%CI: 0.076–0.85, P = 0.026). Furthermore, knowledge scores (OR = 2.0, 95%CI: 1.4–2.8, P = 0.00015) and barrier scores (OR = 1.6, 95%CI: 1.3–2.0, P = 6.5e − 5) were both positively related to behavior scores (Fig. 2A).

Fig. 2.

Forest plot; A relative factor associated with behavior score (OR and 95%CI); B relative factor associated with attitude score (OR and 95%CI); C relative factor associated with knowledge score (OR and 95%CI); D relative factor associated with total score (OR and 95%CI). OR, odd ratio; FP, fertility preservation; patients’ sex: the perception that “Parents of girls care more about FP”; financial status: the perception that “Poor parents care less about FP”; active inquiry: the frequency that “Parents ask me about the impact of cancer treatment on their fertility”; FP charge: who should predominate the arrangement of child FP; Barrier 1: patients are too ill to get survival or to delay immediate treatment for FP; Barrier 2: patients cannot afford cost for FP; Barrier 3: parents are not willing to discuss FP; Barrier 4: there is no access to resort of FP; Barrier 5: heavy clinical work load causes lack of time to care about FP; Barrier 6: FP discussion may lead to treatment reluctance on malignancy

Attitude evaluation

Most respondents expressed the desire for professional training (89.01%) and a targeted national guideline (90.35%) for FP, and 90.88% recognized the obligation to inform patients and their parents regarding issues of FP. A total of 69.17% of the respondents agreed to the importance of emphasizing fertility impairment in pediatric cancer treatment. Additionally, 51.21% still insisted in recommending FP for those high-risk patients, while 75.60% affirmed the priority of treatment for cancer as an obstacle in fulfilling FP procedures. A total of 33.78% of the respondents considered that it was meaningless for patients with a poor prognosis to pursue FP. Few respondents answered that a poor financial status of the patients’ family would stop them discussing FP with the patients, and 46.11% of them considered that poverty decreased the patients’ enthusiasm in pursuing FP. In 41.02% of the respondents, they replied that parents of girls cared more about FP than their counterparts of boys.

Those who had religious beliefs (OR = 0.21, 95%CI: 0.058–0.79, P = 0.021) or bore the consideration of “Patients are too ill to survive or to delay immediate treatment for FP” as the major barrier (OR = 4.4, 95%CI: 0.24–0.82, P = 0.0098) tended to have lower attitude score. Those who completely disagreed (OR = 13, 95%CI: 2.0–86, P = 0.0071) or completely agreed (OR = 12, 95%CI: 4.5–30, P = 5.2e–7) with the conception that “Parents of girls care more about FP” had higher attitude scores. Higher attitude scores were also associated with higher barrier score (OR = 1.2, 95%CI: 1.1–1.4, P = 0.0015), having one or more children (OR = 3.3, 95%CI: 1.4–7.6, P = 0.0053), and a “usually” or higher frequency of receiving active consulting of FP from patients (OR = 2.9, 95%CI: 1.2–6.6, P = 0.015) (Fig. 2B).

Knowledge evaluation

The majority of respondents showed high confidence and accuracy of their knowledge on reproductive impairment from antitumor treatment. However, 55.50% of these medical workers did not realize the higher risk of reproductive impairment in boys than in girls. 52.55% of the respondents did not know the fact that ovarian cryopreservation and transplantation were almost the only available measures for girls before adolescence. General surgeons (OR = 0.56, 95%CI: 0.39–0.81, P = 0.0019) and general physicians (OR = 0.43, 95%CI: 0.29–0.65, P = 6.5e − 5) performed significantly worse in the knowledge part. Respondents who chose “surgeon” (OR = 0.59, 95%CI: 0.39–0.89, P = 0.012) to be responsible for FP had worse knowledge scores. Those who chose that “Parents are not willing to discuss FP” as the most primary barrier had poorer knowledge (OR = 0.49, 95%CI: 0.25–0.93, P = 0.030). Participants who had over 5 years of working experience had better knowledge (OR = 2.0, 95%CI: 1.3–3.0, P = 0.0026). The options “agree” or “completely agree” (OR = 1.4, 95%CI: 1.0–1.9, P = 0.034) with the perception that “Poor parents care less about FP” were also associated with higher knowledge scores. Behavior scores (OR = 1.04, 95%CI: 1.01–1.06, P = 0.0017) and attitude scores (OR = 1.06, 95%CI: 1.01–1.11, P = 0.011) were both positively related to knowledge scores (Fig. 2C).

Factors associated with the FP total score

Higher total scores were associated with higher education level of a Doctoral degree (OR = 43, 95%CI: 7.4–250, P = 3.5e − 5), elder age (over 30 years old to younger, OR = 45, 95%CI: 2.1–990, P = 0.015; over 40 years old to younger, OR = 12, 95%CI: 2.2–68, P = 0.0040), having over 20 colleagues (OR = 170, 95%CI: 15–2000, P = 3.9e − 5), and working in a hospital with radiotherapy (OR = 21, 95%CI: 3.7–118, P = 0.00061). Those who reported more frequently be consulted by patients about FP also had higher total scores (“seldom” or higher to “never”, OR = 630, 95%CI: 20–19000, P = 0.00025; “sometimes” or higher to “seldom” or lower, OR = 11, 95%CI: 1.9–69, P = 0.0085; usually to sometimes, OR = 26, 95%CI: 2.6–250, P = 0.0058). Respondents who chose “lack of time” as the primary barrier tended to have a lower total score (OR = 0.017, 95%CI: 4.8e − 4–0.57, P = 0.023). The perception that “a reproductive medicine specialist should take charge of FP” was also associated with a lower total score (OR = 0.039, 95%CI: 0.0068–0.22, P = 0.0028). Respondents from Northeast China appeared to care less about FP overall (OR = 0.026, 95%CI: 0.0027–0.25, P = 0.0017). Details are shown in Fig. 2D. The total score and knowledge score, as well as the single score representing how often the respondents received active counseling about FP from patients’ parents, showed a trend towards an aggregation geographic distribution (Fig. 3A–C).

Fig. 3.

Spatial autocorrelation analysis; A aggregation pattern of the total score; B aggregation pattern of the knowledge score; C aggregation pattern of frequency of patients/parents’ inquiry of FP actively. FP, fertility preservation

Discussion

In recent years, the long-term survival of Chinese pediatric patients with cancer has approached that in advanced countries[13–17]. Development of the prognosis has led to a further strengthened focus on FP. An increasing number of doctors have realized that irreversible impairment of gonadotoxic treatment progressively occurs, which leads to patients and their families suffering physically and psychologically over time. International guidelines recommend that healthcare providers initiate discussion regarding the effect of treatment on fertility with patients with cancer of reproductive age or with parents/legal guardians of children as early as possible in the treatment process. FP-associated concepts are supposed to be emphasized throughout the whole treatment course, and medical professionals’ subjective ideology plays a role in successful fulfillment of FP procedures. To date, few studies have focused on evaluation of knowledge or the attitude of pediatric oncologists. Previous similar surveys on physicians who specialize in adult cancer showed unsatisfactory initiative and executive force in fulfilling FP in China[18]. In addition, regarding the fact that FP-associated concepts were introduced to adult patients with cancer almost 10 years earlier than those to pediatric patients in China, how China’s medical specialists nationwide truly identify or accept the literature recommendations in their daily work should be addressed. This study is the first to investigate how pediatric oncologists in China view FP, which will hopefully help improve the knowledge and attitude of FP more directly.

According to a UK study in 2008, the effect of cancer treatment on fertility was discussed with 63% of patients[19]. In 2017, approximately 60% of physicians stated that they often discussed the treatment’s effect on fertility in Sweden [20]. The proportion of physicians who discussed the treatment’s effect on fertility in our study is much lower than that in this previous study. A previous study has showed such a difference regarding FP discussion across different settings[21]. Surprisingly, although most respondents were relatively familiar with the potential risk of fertility impairment in treatment and positive regarding training and a guideline of FP treatment, they seldomly started an FP-related discussion within their scope. Similar to previous studies[22, 23], a large percentage of clinicians took for granted that survival was the top priority. The majority of the respondents showed concerns regarding at least one of the six statements on barriers in FP. Similar to findings in most previous studies, “the patient’s prognosis and requirement of immediately starting treatment” was the most recognized and even the only factor that those respondents cared. In addition to clinical considerations, clinicians make assumptions about their patients’ priorities and interest in FP based on their own sense of values, which might conflict with the patients’ preferences. In our survey, although only 7% of respondents viewed “cost” as the primary barrier, 36.5% of them mentioned “cost” as a barrier factor. Agreement with the perception that “the financial status would affect FP” was associated with more complaints in barriers. According to a previous study, females from poor financial status were at higher risk of FP deprivation[24–26]. In our study, an interesting new problem arose that a total of 46.11% of the respondents agreed with the perception that “Parents of girls care more about FP than those of boys.” This finding is consistent with the finding that most respondents did not believe that “Men were more susceptible to reproductive toxicity than women” in the assessment of knowledge. Given that many participants offer passive discussion according to patients’ inquiries, such prejudice made potential FP requirement of certain patients like males from poor families at the risk of being neglected.

A higher education level, more working experience, or larger hospital scales were associated with higher behavior score, attitude score, knowledge score, and barrier scores. These findings suggested that FP received attention from more educated specialists in more authorized centers. However, these findings raise the concern that an uneven distribution of medical resources exposed many patients to a higher risk of fertility impairment. In fact, we found an interesting geographical aggregational trend in the distribution of the total score and knowledge score. Specifically, respondents from Northeast China performed worse, which further testified the unevenness. Such a phenomenon may be explained by the fact that academic associations are often established by region, which regulate clinical treatments for their members according to uniform standards.

We noticed that general surgeon and physicians performed significantly worse in FP knowledge than oncological surgeons and hematologists, which implied that FP arrangement would benefit from subdivision of medical specializations. In addition, the frequency of patients/parents’ active inquiries was positively associated with the behavior score, attitude score, and total score, which implied a trend of judgment regarding the patients’ preference was prevalent among the respondents. In other words, ignorance on the patients’ side and passivity on the medical specialists’ side both contributed to the poor performance of FP discussion in China.

When the respondents were asked who should predominate FP in multidisciplinary collaboration, physicians picked hematologists as the most proper one, but opposed the choice of surgeons. Those who supported oncological surgeons or reproductive medicine specialists turned out to have lower score in behavior, attitude, or knowledge part. In China, oncological surgery and hematology are usually two independent departments. The Oncological Surgery Department may be a good choice for predominating FP arrangement because most FP-associated treatments are surgical procedures. However, only 35% of the surgeons identified themselves as the choice to be responsible for FP arrangement. The self-perception of oncological surgeons cannot match the potential expectations and demands. On the other hand, surgeons showed little willingness to follow physicians as the physicians expected in FP, since only 27% of the surgeons chose hematologist as the proper one in charge. Therefore, there is increasing obstruction in multidisciplinary cooperation regarding FP.

This study is limited by a comparatively small sample size and over 25% of drop-out rate, which may cause potential deviation in the analysis. In addition, this survey only investigated the self-reporting picture of medical workers, and therefore some results especially those regarding patients’ perceptions may reflect part of but not exactly be the truth. In order to get more precise information of pediatric FP in China, further investigation towards both the medical workers and the patients on a larger scale are required.

Conclusion

Although Chinese oncologists generally bear positive attitude towards FP in pediatric patients, they seldom carry out FP discussion during daily clinical practice. Three problems exist among most participants, namely misunderstanding of FP knowledge, lack of multidisciplinary cooperation, and conducting FP discussion serving the patients’ preference rather than as an obligation. These results suggest the requirement for standard training programs and guidelines conducted by multidisciplinary teams for medical workers. To the best of our knowledge, this is the first study to address the topic of FP in pediatric patients with cancer in China. Our findings should provide useful information for optimizing the flow path and facilitating further scientific research and education on FP in China.

Funding

Shanghai Hospital Development Center Foundation (SHDC220222306 and SHDC12024128) and Shanghai Jiao Tong University the Medico-engineering Crossover Project (YG2022QN093).

Data availability

Data is available upon reasonable request to Yuhua Shan and Dapeng Jiang.

Declarations

Ethical approval

This research complied with the guidelines for human studies and was conducted ethically in accordance with the World Medical Association Declaration of Helsinki. The study protocol was approved by the institute’s committee on human research.

Study approval

This study protocol was reviewed and approved by IRB of Shanghai Children’s Medical Center Affiliated to Shanghai Jiao Tong University School of Medicine, approval number [SCMCIRB-K2022181-1].

Competing interests

The authors declare no competing interests.