Multidisciplinary evaluation improves prevalence of testis-sparing surgery in children with testicular benign tumors: a cross-section study

Abstract

Objective

To investigate the profile of children with benign testicular tumors and compare the prevalence of testis-sparing surgery (TSS) in two periods.

Materials and methods

Data from children with testicular benign tumors who were admitted to our hospital from January 2004 to March 2024 were retrospectively retrieved and multidisciplinary evaluation was administered beginning in 2018. Statistical analysis was performed to analyze the factors associated with TSS.

Results

There were 51 children with benign tumors, including 24 with teratomas, 21 with epidermoid cysts, 3 with adenomas, 2 with mesothelial cysts and 1 with sex cord–stromal tumor. Four patients had elevated serum AFP levels, and preoperative ultrasound examination of 5 patients revealed malignant tumors with normal tumor markers. Twenty-six patients underwent TSS, and frozen-section examination was performed in 18 patients, which was consistent with the final pathological results. Since 2018, the proportion of TSS increased significantly compared with that in the previous period(19/25 vs. 7/26, p < 0.001). Multiparameter analysis revealed that tumor size and period were significantly associated with TSS (p = 0.002 and 0.002, respectively). The median follow-up time was 44 months, and none of the interviewed patients experienced any complications. The median sizes of the healthy testis and the involved testis were 26 mm and 23 mm, respectively. A > 10 mm difference in testis size was detected in 2 patients.

Conclusions

The overtreatment of pediatric testicular benign tumors is not uncommon. A comprehensive evaluation should be conducted, and testis-sparing surgery should be considered if feasible. Children seem to have similar sized testes after testis-sparing surgery.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12885-026-15937-z.

Introduction

Testicular tumors are among the most common solid tumors in children, and their incidence rate is approximately 0.5–2.0/100 000 [1–3]. Owing to their rarity, the treatment of these tumors often follows the same guidance as their adult counterparts do, and benign testicular tumors are frequently overlooked. In recent decades, studies have shown that benign testicular tumors are more common in children than in adults, which has had a significant impact on the treatment of pediatric testicular tumors [1, 4–7]. Many studies have shown that testis-sparing surgery (TSS) can effectively remove tumors and preserve normal testicular tissue. Therefore, precise preoperative evaluation is crucial for individual treatment [8–11].

Tumor size is crucial to TSS, and the guidelines for testicular cancer indicate that a testicular mass less than 2 cm in size is eligible for TSS [12, 13]. In 2017, we reported that the prevalence of TSS differed between medical centers and time periods for reasons other than size, and multidisciplinary evaluation of small testicular tumors has been performed in our center since 2018 [14]. Our recent research revealed that anatomical characteristics (SAVE score) could simplify the evaluation for TSS [15]. In addition to these factors, the surgeon’s opinion might also affect the popularity of TSS and lead to the overtreatment of children with benign testicular tumors. A retrospective analysis was performed to explore the profiles of children with benign testicular tumors in our center and compare the proportions of TSS between two time periods.

Materials and methods

From January 2004 to March 2024, 212 children with testicular tumors were admitted to Sun Yat-sen University Cancer Center. The distribution of pathological histology is presented in Fig. 1, and a total of 51 patients with benign testicular tumors were included in this study. The serum levels of alpha fetoprotein (AFP) (normal range 0.00–25.00 ng/mL) and beta human chorionic gonadotropin (β-HCG) (normal range 0.00–3.00 mIU/mL) were measured via the electrochemiluminescence method. All patients underwent testicular ultrasound examination before surgery, and 5 patients underwent abdominal and pelvic CT examinations.

Fig. 1.

The histological distribution of testicular tumors. YST: Yolk sac tumor; MT: Mature teratoma; EC: Epidermoid cyst; ERMS: Embryonal rhabdomyosarcoma

From 2018 to the present, for children with uncertain small testicular tumors, multidisciplinary evaluation, including physical examination, serum levels of AFP and β-HCG by a urologist, detailed ultrasound characteristics (boundary, echo features, blood flow and enhanced status of the testicular tumor, volume of normal testicular tissues) by a sonographer, intraoperative ultrasound evaluation and surgical detection by a urologist, and frozen-section examination (FSE) and final pathological results by a pathologist, was needed.

The patients underwent TSS according to the FSE, and informed consent from parents was acquired prior to surgery. Some patients with typical ultrasound features of benign tumors underwent TSS without comprehensive evaluation. All patients underwent surgery via the inguinal approach. For children with malignant testicular tumors, 5 underwent transformation from TSS to radical orchiectomy (RO) due to malignant FSE results, which were consistent with the final pathological reports. All 161 children with testicular malignant tumors underwent RO. For patients with benign tumors, 1 child transformed to RO due to insufficient normal tissue with a tumor size of 2.7 cm. In all, 25 patients underwent RO, and 26 patients underwent TSS.

Regular outpatient follow-up was needed. All patients with testicular benign tumors were advised to attend a follow-up every six months and then undergo regular telephone interviews annually. The last follow-up was in October 2024, and the general status of the child, growth and development, recent physical examination, and scrotal and/or retroperitoneal ultrasound examination results were recorded.

Results

Among the 51 pediatric patients, 21 presented with tumors on the left side, 28 presented with tumors on the right side, and 2 presented with tumors on both sides. The ages of the patients ranged from 3 months to 14 years, with a median age of 9 years and 14 patients were aged 2 years or younger. The maximum diameter of the tumors was 0.4–5.4 cm, with a median size of 1.8 cm. Preoperative ultrasound revealed high or uneven echoes in 49 patients, low echoes in 2 patients, clear boundaries in 42 patients, and unclear boundaries in 9 patients (Tables 1 and 1S). A total of 25 children underwent RO, and 26 underwent TSS. The patients in the RO group had larger tumors (p = 0.001), and the proportion of patients thatwho received TSS significantly increased since 2018 compared to the previous period (19/25 vs. 7/26, p < 0.001). Logistic analysis revealed that tumor size and period were independent predictors of TSS (p = 0.002 and 0.002, respectively) (Table 2).

Table 1.

Characteristics of patients divided by the year of 2018

	Before 2018(26)	2018 and later(25)	P
Age(year)	7.0(0.2 ~ 14.0)	9.0(0.3 ~ 14.0)	0.224
Age (≤ 2 years old)	10	4	0.072
Max diameter(cm)	2.0(0.4 ~ 5.4)	1.7(0.7 ~ 3.6)	0.406
Max diameter(≤ 2.0 cm)	14	17	0.301
TSS	7	19	< 0.001
Elevated serum AFP level	3	1	0.610
Unclear boundary in US	4	5	0.726
Clinical diagnosis of malignant tumor	2	3	0.668
FSE	4	14	0.002

TSS testis sparing surgery, US ultrasound examination, FSE frozen-section examination

Table 2.

Logistic regressive analysis of surgical approach

Factors	Univariate	Multivariate
	P value	Wals	Hazard ratios (95% CI)	P value
Age	0.185	1.162	0.411(0.066–2.541)	0.338
Max diameter	0.001	10.617	0.046(0.007–0.313)	0.002
Clinical diagnosis of malignant tumor	0.608
Elevated serum AFP level	0.303
Period	0.001	8.521	16.272(2.873–92.175)	0.002

Frozen-section examination (FSE), which has been much more common since 2018, was performed in 18 patients, (14/25 vs. 4/26, p = 0.002) (Table 1), and all the results revealed benign tumors that were concordant with the final pathological reports. The final pathological results revealed 24 cases of teratoma, 21 cases of epidermoid cysts, 3 cases of adenoma, 2 cases of mesothelial cysts and 1 case of sex cord–stromal tumor. The proportions of TSS in each group are listed in Fig. 2. The two bilateral testicular tumors had the same histological type and included epidermoid cysts and mesothelial cysts. Four children had elevated AFP levels ranging from 60 to 830 ng/mL, their ages ranged from 3 to 5 months, and the tumor sizes ranged from 2.2 to 3.9 cm. Ultrasound examination revealed benign tumors, and 1 patient underwent TSS. Postoperative pathology revealed 4 cases of mature teratoma. For 5 patients with suspected malignant tumors on preoperative ultrasound examination, their tumor marker levels were normal, their ages ranged from 1 to 10 years, and their tumor sizes ranged from 1.7 to 2.7 cm. Among them, 2 patients underwent TSS. Postoperative pathological results revealed mature teratomas and epidermoid cysts. One patient in the RO group underwent intraoperative FSE, which revealed a benign tumor with a maximum diameter of 2.7 cm. Owing to the lack of residual normal testicular tissue, radical surgery was performed, and the final pathological result was a mature teratoma.

Fig. 2.

The proportions of TSS in children with different testicular tumors. TSS: testis-sparing surgery, RO: radical orchiectomy

The follow-up time ranged from 6 to 87 months, with a median time of 44 months. No interviewed patients had any complications, such as tumor recurrence or testicular atrophy. For the 26 children who underwent TSS, the size of the healthy testis ranged from 14 to 45 mm, with a median of 26 mm, and the size of the involved testis ranged from 13 to 45 mm, with a median of 23 mm. A > 5 mm difference in size was detected in 7 patients, and a > 10 mm difference in size was detected in 2 patients (8.0%).

Discussion

The most common malignant testicular tumor in children is a pure yolk sac tumor, while the others are almost all benign tumors, such as teratomas, which are the most common [4, 6, 7]. In 2012, our research reported 37 cases (34%) of benign testicular tumors and 32 cases (29%) of mature teratomas in children; these numbers are slightly lower than those reported in the European and American literature but similar to those reported in South Korea, which might be related to regional distribution differences [1, 4, 6]. Testis-sparing surgery (TSS) is a safe and reliable treatment for benign testicular tumors in children. However, owing to the rarity of such tumors, they are often treated via radical surgery as adult testicular cancers would be, which ultimately leads to overtreatment [9, 14–18]. In perioperative evaluation, testicular ultrasound and serum AFP levels play important roles in the diagnosis of testicular tumors in children. The vast majority of pediatric testicular tumors with normal AFP levels are benign tumors. However, for children under 1 year of age who could have physiologically elevated serum AFP levels, even if there is an increased serum AFP level, the possibility of benign tumors should still be considered in combination with ultrasound examination to avoid misdiagnosis and mistreatment [4, 6, 19, 20]. Hence, multidisciplinary preoperative evaluation should be conducted to avoid overlooking benign testicular tumors in children.

In this study, the proportion of benign tumors in children with testicular tumors was approximately 25%. With comprehensive evaluation before surgery, the prevalence of TSS has increased significantly since 2018 (19/25 vs. 7/26). For the 4 infants with elevated serum AFP levels, ultrasound examinations revealed clear boundaries. Owing to the unpopularity of TSS prior to 2018 and the large tumor sizes, 3 of these patients underwent radical surgery, and postoperative pathology revealed mature teratomas. Moreover, the consistency between the intraoperative frozen-section examination (FSE) results and the postoperative pathological results was favorable; 18 patients with benign tumors and 5 patients with malignant tumors were detected. For patients with indeterminate diagnoses, intraoperative FSE played a critical role in surgical decisions. For patients who underwent TSS, 9 didn’t undergo FSE, and their diagnosis relied on ultrasound for those tumors with typical ultrasound features. As multidisciplinary evaluation developed, FSE was required for all patients who underwent TSS. Children with testicular teratomas were associated with a lower proportion of TSS than children with epidermoid cysts (9/24 vs. 13/21). This difference might be derived from the preoperative evaluation and diagnosis of various types of testicular tumors., Patients with epidermoid cysts can often be confirmed by ultrasound examination.

With the development of imaging, the preoperative diagnosis of testicular tumors has become more accurate, making it easier to screen for benign pediatric testicular tumors [21, 22]. In addition to testicular cancer markers, including AFP, β-HCG and LDH, some serum parameters might also be helpful in differentiating benign and malignant testicular tumors [23]. However, FSE is the standard protocol for patients undergoing TSS. Hence, for children with indeterminate testicular tumors, TSS and FSE should be considered with multidisciplinary evaluation, and unnecessary radical surgery should be avoided to reduce the physiological and psychological impacts on patients that are associated with comprehensive evaluation [14, 24]. The recent consensus among pediatric urology experts also suggested that TSS should be the first choice for testicular tumors that are not clearly diagnosed as malignant [19].

During follow-up, we also found that most children (19/26) had similar sizes of bilateral testes. This result may be due to the use of testis-sparing surgery and the process of testis development. Regardless, testis-sparing surgery is feasible for resecting benign testicular tumors and allows for the retention of a sufficient amount of testicular tissue. To the best of our knowledge, this is the first report on size differences after testis-sparing surgery, and children seemed to have similar sizes of testes during follow-up. Unlike patients who undergo RO and chemotherapy, the growth of the testis is not impaired by TSS for most children [25]. Especially for infant patients, the volume of the testis is minimal, and normal tissue adjacent to the tumor is often compressed so thin that it can’t be precisely detected by ultrasound. When the tumor is enucleated, the compressed testis tissue enlarges during surgery. This implies that TSS should be performed for children with benign testicular tumor as feasibly as possible, regardless of tumor size.

In the past decade, it has been reported that benign tumors are not uncommon among pediatric testicular tumors. Although TSS has been recommended for indeterminate testicular masses in guidelines, most patients with testicular tumors undergo radical surgery at elementary medical centers. Overall, preoperative evaluation and advocating for TSS are still needed. We believe that multidisciplinary evaluation should be performed and that TSS should be considered for patients with indeterminate testicular tumors to preserve testicular function as much as possible. In addition to multidisciplinary factors, size was a significant factor for TSS failure in this study (p = 0.002). Moreover, with the help of objective evaluation tools, TSS candidates can be effectively screened utilizing this process [15]. For some complicated cases during operations, such as deep positioning or proximity to the hilum, intraoperative ultrasound was used to mark the boundary of the tumor, and enucleation of the tumor was performed to preserve adjacent tissue and blood vessels. However, all surgical procedures were based on the clinical decision regarding TSS.

As a retrospective analysis, this study has its limitations: the decision of choosing RO was complicated, and some significant factors might not have been taken into consideration. Some patients with benign tumors might undergo surgery at local elementary medical centers, while patients with malignant tumors are transferred to our center. This process could lead to bias and decrease the proportion of benign tumors in our center. However, to the best of our knowledge, benign testicular tumors are not uncommon in children, and the prevalence of TSS has increased significantly with multidisciplinary evaluation.

Conclusions

Benign tumors account for a high proportion of testicular tumors in children, and the sizes of testes after testis-sparing surgery appear to be similar. Testis-sparing surgery could be performed in combination with multidisciplinary evaluation for those diagnosed with benign or indeterminate testicular tumors.

Authors’ contributions

YYL and QZK were responsible for data collection and analysis, interpretation of the results, and writing the manuscript. GB, BWJ and LZH were responsible for conducting the study design, data analysis and interpretation. All authors reviewed the final manuscript.

Funding

No funding supported this study.

Data availability

The key raw data has been doposited in the Research Data Deposit public platform (https://www.researchdata.org.cn), with the approval RDD number as RDDA2024189367.

Declarations

Ethics approval and consent to participate

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Due to the retrospective nature of this study, informed consent was exempted (Ethics committee of Sun Yat-sen University Cancer Center). Ethics approval by our Institutional Review Board was obtained and the data were used confidentially for research work (Ethics committee of Sun Yat-sen University Cancer Center: B2017-053-01).

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.