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Department of Pediatric Surgery, Skåne University Hospital, Lund, SwedenDepartment of Clinical Sciences, Pediatrics, Lund University, Lasarettsgatan 48, 221 85, Lund, Sweden
Department of Pediatric Surgery, Skåne University Hospital, Lund, SwedenDepartment of Clinical Sciences, Pediatrics, Lund University, Lasarettsgatan 48, 221 85, Lund, Sweden
Department of Pediatric Surgery, Skåne University Hospital, Lund, SwedenDepartment of Clinical Sciences, Pediatrics, Lund University, Lasarettsgatan 48, 221 85, Lund, Sweden
Accurate referral of boys with suspected undescended testes (UDT) is of importance to preserve fertility and reduce risk of future testicular cancer. While late referral is well studied, there is less knowledge about incorrect referrals, hence, referral of boys with normal testes.
Objective
To evaluate the proportion of UDT referrals that did not lead to surgery or follow-up, and to assess risk factors for referral of boys with normal testes.
Study design
All UDT referrals to a tertiary center of pediatric surgery during 2019–2020 were retrospectively assessed. Only children with suspected UDT in the referral (not suspected retractile testicles) were included. Primary outcome was normal testes at examination by a pediatric urologist. Independent variables were age, season, region of residence, referring care unit, referrer's educational level, referrer's findings, and ultrasound result. Risk factors for not needing surgery/follow-up were assessed with logistic regression and presented as adjusted odds ratios with a 95% confidence interval (aOR, [95% CI]).
Results
A total of 378 out of 740 included boys (51.1%) had normal testes. Patients >4 years (aOR 0,53, 95% CI [0,30-0,94]), referrals from pediatric clinics (aOR 0.27, 95% CI [0.14–0.51]) or surgery clinics (aOR 0.06, 95% CI [0.01–0.38]) had lower risk of normal testes. Boys referred during spring (aOR 1.80, 95% CI [1.06–3.05]), by a non-specialist physician (aOR 1.58, 95% CI [1.01–2.48]) or referrer's description of bilateral UDT (aOR 2.34, 95% CI [1.58–3.45]), or retractile testes (aOR 6.99, 95% CI [3.61–13.55]) had higher risk of not needing surgery/follow-up. None of the referred boys that had normal testes had been re-admitted at the end of this study (October 2022).
Discussion
Over 50% of boys referred for UDT had normal testes. This is higher or equal to previous reports. Efforts to reduce this rate should in our setting probably be directed towards well-child centers and training in examination of testicles. The main limitation of this study is the retrospective design and the rather short follow-up time, which however should have very modest effect on the main findings.
Conclusion
Graphical AbstractDistribution of referrer's findings by diagnosis set by a pediatric surgeon in boys referred for undescended testes.
]. On one hand, it is relatively common with late referrals, resulting in lower adherence of timely surgery, which ultimately may put the boy in higher risk of infertility and malignancy later in life [
]. Another problem is what you might call unnecessary referrals, i.e. the boy has completely normal testicles when examined by a pediatric surgeon or urologist. While this may not physically harm the boy, it will cause unnecessary concern among the boys and caregivers. It will also, since UDT is very common, take valuable time and cost from the health care system. Previous, mainly US and Asia based studies [
] have highlighted the high prevalence of unnecessary referrals and risk factors for it, such as the boys age and socioeconomic factors but also factors increasing the odds of the boy having a true UDT [
A few years ago, because of a rising number of referrals, our center started with specific outpatient clinic days with only suspected UDT. It then became more obvious that a high number of boys had a completely normal examination. Our hypothesis for this study was that around 75% of all referrals were of boys with normal testicles. By identifying predicting factors for UDT diagnosis in the referral to a secondary or tertiary care, targeted efforts can improve the quality and coordination of UDT care in Sweden. Increased accuracy of UDT referrals would mean fewer unnecessary testicular examinations, less anxiety for parents and children, decreased suppression effect on other patient groups, and decreased costs for the health care (especially since children's outpatient care is free of charge).
The aim of this study was to determine the proportion that does not need surgery or further follow-up for undescended testes out of all children referred to a tertiary pediatric surgery center. Further, the aim was to see how demographic, referral-related and geographic factors are reflected in referral patterns.
Methods
The study was approved by the regional ethical board (Ref. no 2010/49), and permission to access medical journals through the hospital's computer system was granted by the KVB consultation (Ref. No 119-19).
Settings and population
Children were assessed at a tertiary center of pediatric surgery where advanced pediatric surgery is performed on children under 15 years of age. The catchment area is the southern healthcare region, which includes the counties Skåne, Kronoberg, Blekinge, and the southern part of Halland, covering approximately 2 million people. Children ≤1 year and all children with unpalpable UDT are referred to Lund for treatment, while older children with ascending testis may be treated at a local hospital in the northern and north east parts of the catchment area. Incoming referrals for UDT are from both primary and secondary care centers.
Data collection
Data collection was done retrospectively. All referrals sent to the section of pediatric urology between 2019 and 01-01 and 2020-12-31 were reviewed, and referrals regarding UDT that had led to a visit to the pediatric surgery department were included. Cases of recurrent UDT in patients previously operated for UDT were considered relapses or a potential surgical complication and therefore excluded. Referrals regarding further control of retractile testicles were also excluded. Hence, only referrals where the referrer specified that they suspected UDT was included. This was based on the clinical question on the written referral. Hence, if the referrer wrote that the referral was for a suspected undescended testis this was defined as a true UDT referral. If the referrer asked for help with control of retractile testis, this referral was not included. At last, if the referrer clearly specified that they suspected UDT but in their examination described findings congruent with a retractile testicle, this was defined as an UDT referral (please see below regarding referrers findings).
The referral letters were carefully reviewed and the following information was retrieved: age, date of referral, patient's zip code, weeks of prematurity, type of referring care unit, referrer's professional title, examination findings described in the referral, and if ultrasound had been done. The journal was thoroughly reviewed regarding the examination done by the pediatric surgeon/urologist, the specific diagnosis set, and if the patient was scheduled for surgery, follow-up, or neither (i.e. normal testes).
Primary outcome
The primary outcome was no need for surgery or follow up, defined as normal testicles during examination by the pediatric surgeon/urologist. No need of follow-up was defined as no need for control of retractile testicles (all these controls are performed at our own center) or no new referral on the same patient to our center up until October 2022. To descriptively compare the findings by the pediatric surgeon, the following categories were used: unilateral UDT, bilateral UDT, retractile testes, and neither UDT nor retractile testes. The latter category implies normal location of the testes.
Independent variables and definitions
Corrected age at referral was computed, with the categories ≤12 months, 13–24 months, 25–36 months, 37–48 months, and >48 months; season of referral was divided into summer (June–August), autumn (September–November), winter (December–February), and spring (March–May); region of residence was categorized based on ZIP codes into Lund/Malmö, southern Skåne, northern Skåne, and outside Skåne (Halland, Småland and Blekinge); type of referring care unit was categorized into well-child center, school health department, primary care center, pediatric clinic, surgery/urology clinic; referrer's educational level was categorized into specialist physician, physician, and nurses; referrer's findings (hence, the testicular examinations findings described by words in the referral) were categorized into unilateral, bilateral, retractile, and others (examination not really described, variations in testicular size or shape, not understandable description, etc.). In cases of inconsistency between the referrer's description of examination findings and the question in the referral, the referrer's findings variable was based on the description of findings from the clinical examination; ultrasound (US) before referral meant an examination initiated by the referrer prior to referral.
Statistics
Descriptive statistics on the percentages of the referrals that led to surgery or follow-up were produced. Chi2-or Fisher's exact test was used to assess differences between the categorical variables. Risk factors for referral of children with normal testes were assessed using binary logistic regression and presented as crude (cOR) and adjusted (aOR) odds ratios with a 95% confidence interval (95% CI). The significance level was set at p < 0.05.
Results
During the study period, 793 referrals concerned UDT of which 26 (3.3%) were regarding previously operated boys, and 27 (3.4%) had missing data, leaving a cohort of 740 included patients (Fig. 1).
Fig. 1Flow chart visualizing the inclusion and exclusion criteria of the study UDT: Undescended testes.
The median age at referral was 18 months. A total of 433 patients (58.5%) were referred from well-child centers and 135 patients (18.2%) were referred from primary care centers. Specialist physician was the most common educational level among referrers (65.5%). Only 65 patients (8.8%) had been examined with ultrasound prior to referral. In total, 235 patients (31.8%) were scheduled for surgery, and 127 patients (17.2%) were scheduled for follow-up, leaving 378 patients (51.1%) with normal testes at examination (Table 1, Fig. 2). None of the referred boys that had normal testes had been re-admitted at the end of this study (October 2022).
Table 1Distribution of referral factors in 740 boys referred to a tertiary center of pediatric surgery for suspicion of undescended testes.
Corrected age at referral
≤12 months
317 (42.8)
13–24 months
83 (11.2)
25–36 months
84 (11.4)
37–48 months
68 (9.2)
>48 months
188 (25.4)
Season of referral
Summer
121 (16.4)
Autumn
227 (30.7)
Winter
171 (23.1)
Spring
221 (29.9)
Region of residence
Malmö/Lund
321 (43.4)
Southern Skåne
209 (28.2)
Northern Skåne
159 (21.5)
Halland, Småland. Blekinge
44 (5.9)
Referring care unit
Well-child center
433 (58.5)
Primary care center
135 (18.2)
Pediatric clinic
98 (13.2)
Surgery clinic
48 (6.5)
Student health department
23 (3.1)
Missing
3 (0.4)
Referrer's educational levela
Specialist physician
485 (65.5)
General medicine
71.5%
Pediatrics
18.1%
Surgery/Urology
10.2
Internal medicine
0.2%
Non-specialist physician
152 (20.5)
Unspecified physician
57 (7.7)
Nurse
42 (5.7)
Pediatric
47.6%
Primary care
38.1%
School
9.5%
Undergraduate
4.8%
Ultrasound before referral
Yes
65 (8.8)
No
675 (91.2)
Values presented as % within category, and as the absolute number and percentage of patients, n (%); (a) 4 missing.
Fig. 2Distribution of referrer's findings by diagnosis set by a pediatric surgeon in boys. referred for undescended testes Big arrow represents the most common diagnosis within each “referrer's finding”. Small arrow represents the second most common diagnosis within each “referrer's finding”, dashed arrows represent the least common diagnoses within each “referrer's finding”. Numbers on arrows represent the absolute number of patients with the indicated finding and diagnosis; UDT: undescended testes; ∗4 patients with referrers finding categorized as “other”; ∗∗ 6 patients with referrers finding categorized as “other”; ∗∗∗12 patients with referrers finding categorized as “other”.
Children with normal testes were, compared to children in need of surgery/follow up, most often referred in the spring, most commonly referred from well-child centers, less often examined with ultrasound, and the referrer's findings consisted more often of bilateral UDT (35.2%) and retractile testes (17.5%) (Table 2).
Table 2Comparison of different referral factors between children in need of surgery or follow and children with normal testes in 740 boys referred for undescended testes.
In the regression analyses; patients over 4 years (aOR 053, 95% CI [0,30–0,94]), referrals from pediatric clinics (aOR 0.27, 95% CI [0.14–0.51]) or surgery clinics (aOR 0.06, 95% CI [0.01–0.38]) had significantly lower risk of not needing surgery or follow-up. Furthermore, patients referred during spring (aOR 1.80, 95% CI [1.06–3.05]), by a non-specialist physician (aOR 1.58, 95% CI [1.01–2.48]) or when the referrer found bilateral UDT (aOR 2.34, 95% CI [1.58–3.45]), or retractile testes (aOR 6.99, 95% CI [3.61–13.55]) had higher risk of not needing surgery or follow-up (i.e. normal testes) (Table 3, Fig. 3).
Table 3Crude and adjusted odds ratios for the association between referral factors and normal testes at examination by a pediatric surgeon (i.e. not needing surgery or follow-up).
Fig. 3Forest plot of adjusted odds ratios for the association between referral factors and normal testes at examination by a pediatric surgeon (i.e. not needing surgery or follow-up) in boys referred for undescended testes.
US was mainly ordered by surgery clinics (56%) and pediatric clinics (32%). Of those boys sent for ultrasound, around 54% were palpable, 28% were non-palpable, 5% were retractile and 9% were normal. US was in the adjusted analysis associated with a substantially lower risk of not needing surgery or follow-up (i.e. normal testes) (aOR 0.22 95% CI [0.07–0.68]) (Table 3, Fig. 3).
Discussion
More than half of boys referred for suspicion of UDT did not need surgery or follow up, i.e. had normal testes. The oldest boys, and boys referred from pediatric or surgical clinics had lower risk of an unnecessary referral, while boys referred during spring, by a non-specialist physician or when the referrer found bilateral UDT or retractile testes, had higher risk of not needing surgery or follow-up (i.e. normal testes).
Early referral is essential to meet the recommendation of surgery before one year of age or as soon as the UDT is detected. Correct referrals enable time-effective management of UDT patients by pediatric surgeons, while excessive referral of healthy patients risks resulting in unnecessary stress among families, and suppression of children with true UDT, with risk of delayed surgery consequently. Out of all referrals to the tertiary center of pediatric surgery in the study, suspicion of UDT was the most common reason for referral. Moreover, around half of the included patients had normal testicular locations and did not need any further follow-up or treatment. This leads to the conclusion that increased accuracy of UDT referrals may save a lot of discomfort, parental anxiety, time, and money. The Swedish well-child checkups are in theory ideal to secure early detection and treatment of UDT. It is also widely adhered to with a 99% participation in the population [
]. However, successful screening requires qualified practitioners. It is fundamental that all referrers can separate UDT from normal testes and know which patients to refer and at what age. Child health care in Sweden is organized so that well-child centers should detect and refer UDT as part of a comprehensive screening for several malformations and diseases [
]. Hence, it is expected that most of the UDT referrals are sent from well-child centers is expected. Unexpectedly, this study also discovered that well-child centers were the most frequent referrers of boys with normal testes and that being referred from a well-child center is a risk factor of being referred with normal testes. False positive results are a common concern regarding screening in general, with consequences such as unnecessary examinations, increased anxiety, etcetera. However, the importance of screening children for UDT is established and measures to improve referral accuracy are desirable [
]. The question of why the most frequent referrer is also the most inaccurate remains to be answered. Differences in management between clinics might have contributed to the results. For example, well-child centers examine testes by routine, while other types of clinics might achieve a higher accuracy by only examining the testes of children searching for testicle-related causes. Furthermore, the extensive examination performed on well-child checkups might result in a cold or discomforted child with retracted testes which makes the examination more difficult. A stressful working climate in primary care has been reported by Anskär et al. [
], and time pressure in combination with challenging examinations and fear of missing a diagnosis with potentially severe sequelae together constitute poor conditions for effective UDT screening. Altogether, there are many potential explanations to what causes the high percentage of referrals of children with normal testes coming from well-child centers. This study suggests that there is a need for improved referral accuracy at well-child centers, possibly through educational efforts. No specific factors that negatively influence the referral accuracy of well-child centers were assessed in this study, but a need for further evaluation of such factors is suggested. At last, parents’ expectations and opinions were not evaluated in this study. There will always be cases were parents would prefer a reassurance from a pediatric surgeon, and referrals of children with worried parents or parents who repeatedly have sought care for suspected UDT, should never be turned down by the tertiary center.
The large proportion of inaccurate referrals (patients with normal testes) seen in this study is similar or slightly higher compared to previous studies. A Canadian study from 2017 found that 51% of patients referred for UDT to a center in Ottawa had normal or retractile testes [
], 52% of patients referred for UDT to a hospital in Oklahoma during 2019–2020 needed surgery, compared to this study where only 31.8% needed surgery. The higher accuracy found by Moran et al. is overshadowed by a high percentage (54%) of patients being referred late (>18 months), which can be compared to 45.7% aged over 13 months in this study. Thus, a relevant question is whether the higher referral accuracy was achieved to the expense of delayed discovery. Awareness of the balancing act between excessive referral and missing the diagnosis is essential when aiming to increase referral accuracy. Educational efforts have potential to improve both referral accuracy and timing. Another very important point is that although the examination of boys in terms of even finding a testicle have a high sensitivity and specificity, the positive predictive value will be very low because of the prevalence of UDT being only around 2%. At the same time, the negative predictive value (NPV) will instead be very high even if the specificity is as low as for example 60% (NPV = 99% if the prevalence is 2%). Since we in this study included retractile testicles in the “non-normal” group, the example above is not completely accurate but it reflects that there will always be some “unnecessary referrals” when the prevalence is low, even if the referrer's examination is relatively good. At the same time; the risk of missing an UDT is instead low because of the low prevalence, almost regardless of the referrer's accuracy. Hence, the risk that a more rigorous referral, after introduction of perhaps an education program or clearer guidelines, would result in many missed UDT is probably low. We still believe, as previously discussed by Snoodgrass et al. [
] that there are measures to be taken to improve the accuracy. For example, if the boy has a normal examination at birth and at six months of age, and symmetrical scrotum, the risk of an UDT among term boys between 1 to around 5 years of age is extremely low, and should perhaps prompt a repeat examination at another time point before a referral is sent. At last, we will in the future try to request the findings from the examination of the testicle at birth on all boys with UDT.
A comparison of the referrer's findings to the final diagnosis received at the pediatric surgery center revealed a low accuracy in referrer's findings, further indicating that educational efforts regarding examination of boys testes are needed. Most patients referred for bilateral UDT or retractile testes had normal testes. Retractile testes are previously described as a risk factor for delayed referral, as well as inaccurate referral [
]. In this study, the impact of retractile testes on age at referral was not assessed, but association with inaccurate referral was confirmed. A potential reason is that even normal testes can retreat up towards the inguinal canal when a child is cold or in discomfort, which can complicate palpation and cause misdiagnosis [
]. However, with a good examination technique, warm hands, and a calm environment, manipulation of the testes into the scrotum should be possible. Furthermore, few patients with referrer's findings of bilateral UDT had UDT, which indicates lack of examination technique. It is plausible that practitioners with deficient technique have the same difficulties on both sides and thus are more likely to write bilateral UDT in the referral, making it a risk factor for referral of children with normal testes. This finding further supports the suggested need of UDT education among referrers.
An increased risk of referral that does not lead to surgery or follow up was seen for non-specialist physicians, compared to specialist physicians. The result is expected since specialist physicians ought to have examined more UDT:s than other physicians. On the other hand, higher dependance on guideline documents among other physicians might keep them better updated on current management and thus improve their referral accuracy. Less experienced practitioners are also more probable to ask colleagues for help in unclear cases. Similar results were seen by Lim et al. [
], suggesting higher experience level of the referrer was associated with better knowledge of UDT management and referral, among practitioners in the UK who responded to a questionnaire about UDT. The risk for attrition bias is however high because less competent practitioners are less likely to respond, and in combination with a low response rate and a non-Swedish setting, the comparability of the study is vastly limited.
The median age at referral found in this study was 18 months, which is three times the recommended age for referral [
]. However, the median age of UDT referral can never reach 6 months because of secondary ascent, which occurs later. The age distribution of all referred patients in this study follows a bimodal curve similar to the distribution of age at surgery previously described in the Swedish population by Bergbrant et al. [
]. However, the second peak in timing of surgery found by Bergbrant et al. is delayed by four years compared to the second peak in timing of referral seen here. They also found big variations of median age at surgery between counties, where the southern health care region was in the lower range, which might contribute to the delay as well as waiting times for diagnosis and surgery. The second peak in referral rates seen at around 36 months might be explained by presence of the cremasteric reflex among most boys by then [
]. Likewise, the crude odds ratios of this study indicate a higher risk of being referred with normal testes for children 25–48 months. Significance is lost in the adjusted model, potentially concealed by a similar effect on the referrer's findings of retractile testes or bilateral UDT caused by presence of the cremasteric reflex mentioned above. Secondary ascent is another possible factor behind the second peak, although previous studies have reported various age distributions of secondary ascent. Dinkelbach et al. [
] found a peak in incidence between 8 and 11 years. Previous reports of high prevalence of secondary ascent complicates the interpretation of late referrals seen in this study [
Some of the patients had been examined with ultrasound prior to referral, even though recommendations are clear that it should not be used as a diagnostic method [
]. The finding of lower odds of referral that does not lead to surgery or follow up for patients examined with ultrasound needs cautious interpretation since only patients with a positive ultrasound result were referred and thus included in the study, and ultrasound is often ordered when the doctor can't find the testicles at all. The use of ultrasound in selecting which patients to refer is shown to increase referral accuracy, however the implementation of this knowledge must be weighed against other factors such as potential delay in referral or treatment, and cost-effectiveness, which is not analyzed here.
A strength of this study is that all referrals received during the two years were assessed for the inclusion and exclusion criteria. Furthermore, all referrals were assessed and transferred into the study protocol by the same person, which decreases the risk for different applications of inclusion and exclusion criteria or interpretation of referrals. The outcome variable, treatment, is clearly stated in the electronic journal with no room for interpretation, which advocates the use of treatment as the main outcome rather than diagnosis. Outcome variables were determined before any data was collected, to avoid reporting bias. One might state that a weakness of the study is that there is no long-term follow-up of the group with normal testes. We can't of course be certain that no boy will return later on with an ascending UDT but we want to emphasize that no retractile testicles (with risk of ascendence) were included in the 51% reported to have normal testes. Another significant limitation is that retrospective assessment of already written referrals and patient journals, allows interpretation by the assessor. In the data collection of this study, the classification of referrer's findings was particularly challenging since the referrer's formulations were sometimes inexplicit. Validity was sought through interpreting the whole text rather than just using the referral's.
Shortcomings in the management of undescended testis: guideline intention vs reality and the underlying causes – insights from the biggest German cohort.
], different type of education such targeted education programs, webinars, letters to referrers, improved guidelines and dissemination of these, and information to parents, can improve the accuracy in the referral of boys with UDT. We will start a new study with a survey directed at doctors at well child centers to evaluate their opinions regarding and management of boys with UDT.
Conclusion
Over half of the UDT-referrals to a tertiary center of pediatric surgery were of boys with normal testicles, meaning no need for surgery or follow up. This corresponds well with previous international studies, and means that there may be a lot to gain from a more effective referral pattern. The results from the present study suggest that education and practice in examination technique targeted primarily at well-child centers may decrease the rate inaccurate referrals. In the light of this, a national survey of UDT management has been launched directed at well-child centers.
Ethical approval
This work has been approved by the regional ethical committee.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Shortcomings in the management of undescended testis: guideline intention vs reality and the underlying causes – insights from the biggest German cohort.
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