Abstract
Few reports have been published regarding the outcomes of patients who develop an undescended testicular malignancy (UTM). Patients with a diagnosis of nonseminomatous or seminomatous testicular cancer were identified in the Surveillance, Epidemiology, and End Results (SEER) database to analyze the sociodemographic and survival outcomes of patients with UTM and those with descended testicular malignancy (DTM). Patients with UTM were more likely to be older, married, a minority or foreign born and to have seminoma, a higher rate of node positivity, and a higher SEER stage compared with patients with DTM.
Background:
Few reports have been published regarding the outcomes of patients who develop an undescended testicular malignancy (UTM). Our objective was to analyze the sociodemographic and survival outcomes of patients with UTM and those of with descended testicular malignancy (DTM).
Patients and Methods:
All 17 registries constituting the Surveillance, Epidemiology, and End Results (SEER) database were analyzed from 1988 to 2008. Patients with a descended or undescended testis and a diagnosis of nonseminomatous or seminomatous testicular cancer were identified. Descriptive statistical data and multivariate analysis were used to identify the predictors of a UTM diagnosis. The primary outcomes were overall and disease-specific survival.
Results:
The study cohort included 10,159 men (95.3%) with DTM and 496 (4.7%) with UTM. Patients with UTM were more likely to be older, married, and a minority or foreign born and to have seminoma, a higher rate of node positivity, and a higher SEER stage compared with patients with DTM. The median survival time for patients with UTM was longer than that for patients with to DTM (83.1 vs. 72.5 months; P = .0001), although no difference was found in cancer-specific mortality (P = .34).
Conclusion:
Patients with UTM are more likely to be a minority or foreign born, highlighting a previously unrecognized healthcare disparity that might represent a lack of diagnosis and access to care.
Keywords: Clinical outcomes, SEER, Socioeconomic factors, Testicular malignancy, Undescended testis
Introduction
In 2014, an estimated 8820 new cases of testicular cancer and an estimated 380 deaths will have occurred in the United States.1 Well-established risk factors for testicular cancer include a family history of testicular cancer, a personal history of testicular cancer, intratubular germ cell neoplasia, and cryptorchidism.2 Recent studies have also suggested that diet and/or other environmental factors might play a role in development of germ cell testicular malignancies.3,4 The rate of new cases diagnosed per 100,000 men is 6.6 white, 4.7 Hispanic, and 1.4 African American annually.5 Previous studies have demonstrated an increased risk of developing testicular cancer for men with a higher socioeconomic status (SES), typically measured by income and/or educational attainment. However, lower levels of education and SES have been linked to later-stage diagnosis and increased mortality.6
Cryptorchidism is a common congenital anomaly, occurring in 1% to 4% of full-term and 1% to 45% of preterm infant males.7 Although the benefits of orchiopexy for cryptorchidism are clear, few reports have been published regarding the outcomes of patients who develop a malignancy in an suggested SES disparities associated with cryptorchidism, we hypothesized that men presenting with an undescended testicular malignancy (UTM) would be of lower SES than were men with a descended testicular malignancy (DTM). Therefore, the objective of the present study was to analyze the demographic, clinicopathologic, and socioeconomic demographic data and the survival outcomes of patients with UTM compared with DTM.
Patients and Methods
Study Population
The study cohort consisted of patients from all 17 registries of the Surveillance, Epidemiology, and End Results (SEER) database from 1988 to 2008. Given that the SEER data are public, de-identified data, institutional review board approval was not required. Patients with DTM or UTM were identified in the SEER database using the primary site code C62.1 and C62.0, respectively. Patients with code C62.9 (testis, not otherwise specified) were not included in the analysis (n = 17,672). Subsequently, using the International Classification of Diseases, Oncology (ICD-O) codes, we identified patients with a diagnosis of either seminoma (ICD-O codes 9061–9063) or nonseminomatous testicular germ cell tumor (ICD-O codes 9070–9071, 9080–9085, 9100–9102) for a study cohort of 10,655 patients.
Description of Covariates
The variables of interest included age, race (African American, white, Hispanic, other, unknown), marital status (married, single/divorced/widowed, unknown), retroperitoneal lymph node dissection (RPLND) (yes vs. no), histologic type (nonseminoma vs. seminoma), American Joint Committee on Cancer (AJCC), 7th edition, tumor classification, pathologic nodal status, SEER stage (local, regional, distant, unstaged), and median overall survival (OS) (censoring date, June 10, 2011). The SES variables of interest included the median census county data for the percentage of educational attainment (< 9th grade vs. less than high school), median family income, percentage of poverty level, percentage of unemployed, percentage of ethnic or racial minority, percentage of foreign born, and rural versus urban status.
Statistical Analysis
Descriptive statistical analyses for the demographic, clinicopathologic, and SES variable comparisons were performed using the t test and χ2 test. Survival estimates were calculated using the Kaplan-Meier method for disease-specific survival stratified by testicular descent. Cox proportional hazard analysis was performed to generate odds ratios (ORs) for the risk factors of a diagnosis of UTM using the clinicopathologic and SES factors. Variables listed as “unknown” were kept in the descriptive statistical tables to demonstrate frequencies, but they were not included in the statistical analysis. To prevent confounding of AJCC stage with SEER stage, only the SEER stage was included in the multivariable analysis. The models were constructed using all pertinent variables, and backward selection was used to find the best fit model. Statistical analyses were performed using SAS, version 9.3 (SAS Institute, Cary, NC). All tests were 2-sided, with statistical significance set at P < .05.
Results
Patient Demographics
The complete listing of patient demographics is included in Table 1. The study cohort included 10,159 men (95.3%) with DTM and 496 (4.7%) with UTM. Patients with UTM were older (median age, 36 vs. 34 years; P ≤ .0001) and more often married (52.0% vs. 47.1%; P = .0495) than were the patients with DTM. Significant differences were found between the 2 groups regarding race (P < .0001), with a greater percentage of African American (6.1% vs. 1.7%) and Hispanic (19.2% vs. 17.3%) men with UTM than DTM.
Table 1.
Demographic and Clinicopathologic Outcomes
| Variable | DTM | UTM | P Value |
|---|---|---|---|
| Patients | 10,159 (95.3) | 496 (4.7) | |
| Age (years) | <.0001 | ||
| Median | 34 | 36 | |
| IQR | 26–41 | 29–43 | |
| Race | <.0001 | ||
| White | 7783 (76.6) | 320 (64.5) | |
| Hispanic | 1753 (17.3) | 95 (19.2) | |
| African American | 168 (1.7) | 30 (6.1) | |
| Other | 370 (3.6) | 47 (9.4) | |
| Unknown | 85 (0.8) | 4 (0.8) | |
| Marital status | .05 | ||
| Married | 4780 (47.1) | 258 (52.0) | |
| SDW | 5092 (50.1) | 229 (46.2) | |
| Unknown | 287 (2.8) | 9 (1.8) | |
| SEER registry | <.0001 | ||
| California (other) | 2676 (26.3) | 87 (17.5) | |
| Los Angeles | 3690 (13.3) | 99 (20.0) | |
| Seattle (Puget Sound) | 181 (1.8) | 30 (6.1) | |
| San Francisco-Oakland | 591 (5.8) | 36 (7.3) | |
| Detroit (metropolitan) | 125 (1.2) | 22 (4.4) | |
| New Jersey | 557 (5.5) | 53 (10.7) | |
| Connecticut | 369 (3.6) | 24 (4.8) | |
| Iowa | 557 (5.5) | 28 (5.6) | |
| Utah | 1353 (13.3) | 21 (4.2) | |
| Atlanta (metropolitan) | 167 (1.6) | 28 (5.7) | |
| San Jose-Monterey | 457 (4.5) | 30 (6.1) | |
| New Mexico | 257 (2.5) | 3 (0.6) | |
| Kentucky | 349 (3.4) | 14 (2.8) | |
| Louisiana | 117 (1.2) | 13 (2.6) | |
| Hawaii | 63 (0.6) | 8 (1.6) | |
| Alaska | 15 (0.2) | 0 (0) | |
| Georgia (rural) | 10 (0.1) | 0 (0) | |
| RPLND | .79 | ||
| Yes | 1463 (14.4) | 69 (13.9) | |
| No | 8654 (85.2) | 423 (85.3) | |
| Unknown | 42 (0.4) | 4 (0.8) | |
| Histologic type | <.0001 | ||
| Seminoma | 5731 (56.4) | 352 (71.0) | |
| Nonseminoma | 4428 (43.6) | 144 (29.0) | |
| T classification | <.0001 | ||
| T0 | 16 (0.2) | 7 (1.4) | |
| T1 | 6266 (61.7) | 274 (55.3) | |
| T2 | 2126 (20.9) | 80 (16.1) | |
| T3 | 501 (4.9) | 18 (3.6) | |
| T4 | 520 (5.1) | 9 (1.8) | |
| Local NOS | 570 (5.6) | 48 (9.7) | |
| Unknown | 160 (1.6) | 6 (1.2) | |
| Pathologic nodal status | .0001 | ||
| Regional | 1596 (15.7) | 67 (13.5) | |
| Distant | 215 (2.1) | 24 (4.8) | |
| None | 6384 (67.3) | 317 (63.9) | |
| Unknown | 1498 (14.8) | 88 (17.8) | |
| SEER stage | .0004 | ||
| Localized | 7199 (70.9) | 319 (64.3) | |
| Regional | 1779 (17.5) | 88 (17.8) | |
| Distant | 1116 (11.0) | 82 (16.5) | |
| Unstaged | 65 (0.6) | 7 (1.4) | |
| Survival | .014 | ||
| Alive | 9246 (91.0) | 445 (89.7) | |
| Other cause mortality | 241 (2.4) | 21 (4.2) | |
| Cancer-specific mortality | 301 (3.0) | 19 (3.9) | |
| Survival (mo) | .0001 | ||
| Median | 72.5 | 83.1 | |
| IQR | 27–102 | 34.5–123 |
Data presented as n (%), unless otherwise noted.
Abbreviations: DTM = descended testicular malignancy; IQR = interquartile range; NOS = not otherwise specified; RPLND = retroperitoneal lymph node dissection; SDW = single/divorced/widowed; SEER = Surveillance, Epidemiology, and End Results; UTM = undescended testicular malignancy.
Clinical and Pathologic Outcomes
Patients with UTM had a greater rate of a diagnosis of seminoma (71.0% vs. 56.4%; P < .0001) than did the patients with DTM (Table 1). Between the 2 groups, the differences in T classification (P < .0001), pathologic nodal status (P = .0001), and SEER stage (P = .0004) were significant. Patients with UTM had a more favorable T classification (T0 in 1.4% vs. 0.2%; T4, 1.8% vs. 5.1%). However, they had worse nodal disease (distant, 4.8% vs. 2.1%) and SEER stage (localized, 64.3% vs. 70.9%; distant, 16.5% vs. 11.0%) compared with patients with DTM. The median survival time for patients with UTM was significantly longer than that for those with DTM (83.1 vs. 72.5 months; P = .0001), although no difference was found in cancer-specific mortality (P = .34; Figure 1).
Figure 1.
Kaplan-Meier Survival Curve for Cancer-Specific Mortality for Patients With Descended and Undescended Testicular Malignancy (P = .34)
Socioeconomic Outcomes
Compared with patients with DTM, those with UTM were from counties with a greater median income ($56,611 vs. $54,143; P < .0001; Table 2). Furthermore, patients with UTM were more commonly living in rural (< 2500 people) or metropolitan (> 1 million people) communities (P < .0001).
Table 2.
Patient Socioeconomic Status
| Variable | DTM | UTM | P Value |
|---|---|---|---|
| Median with <9th grade education (%) | 9.3 | 9.0 | .19 |
| Median without high school degree (%) | 20.4 | 20.1 | .43 |
| Median family income ($) | 54,143 | 56,611 | <.0001 |
| Median families < poverty line (%) | 9.4 | 9.2 | .18 |
| Median unemployed (%) | 6.4 | 6.3 | .24 |
| Median minority (%) | 40.4 | 41.8 | .18 |
| Median foreign born (%) | 19.8 | 19.9 | .96 |
| Rural/urban status | <.0001 | ||
| Metropolitan >1,000,000 | 6118 (60.3) | 356 (71.8) | |
| Metropolitan 250,000–1,000,000 | 2629 (25.9) | 85 (17.1) | |
| Metropolitan <250,000 | 634 (6.3) | 25 (5.1) | |
| Urban 2500–20,000 | 407 (4.0) | 12 (2.4) | |
| Urban >20,000 | 283 (2.8) | 13 (2.6) | |
| Rural <2500 | 73 (0.7) | 5 (1.0) |
Data presented as n (%), unless otherwise noted.
Abbreviations: DTM = descended testicular malignancy; IQR = interquartile range; UTM = undescended testicular malignancy.
Predictors of UTM Diagnosis
On multivariable analysis, after adjusting for race, age, RPLND, histologic type, and SEER stage, the significant factors associated with a UTM diagnosis included seminoma histologic type (OR, 2.58; 95% confidence interval [CI], 2.05–3.25), RPLND (OR, 1.40; 95% CI, 1.06–1.87), and SEER stage (OR, 1.44; 95% CI, 1.26–1.64; for a 1-unit increase in SEER stage—localized to regional, regional to distant). The factors that were protective against a diagnosis of UTM included white race (vs. nonwhite; OR, 0.31; 95% CI, 0.24–0.41) and Hispanic race (vs. non-Hispanic; OR, 0.40; 95% CI, 0.29–0.56). After adjusting for socioeconomic factors, residing in a county with more foreign-born inhabitants (highest quartile vs. lowest quartile, OR, 1.33; 95% CI, 1.01–1.76) was associated with a diagnosis of UTM (Table 3).
Table 3.
Factors Associated With a Diagnosis of an Undescended Testicular Malignancy
| Variable | OR (95% CI) |
|---|---|
| Clinicopathologica | |
| Race | |
| White versus nonwhite | 0.31 (0.24–0.41) |
| Hispanic versus non-Hispanic | 0.40 (0.29–0.56) |
| Histologic type | |
| Nonseminoma | Reference |
| Seminoma | 2.58 (2.05–3.25) |
| RPLND | |
| No | Reference |
| Yes | 1.40 (1.06–1.87) |
| SEER stageb | 1.44 (1.26–1.64) |
| Socioeconomic variablec | |
| Percentage foreign born | |
| IQR 1 | Reference |
| IQR 2 | 0.75 (0.57–0.98) |
| IQR 3 | 0.99 (0.75–1.33) |
| IQR 4 | 1.33 (1.01–1.76) |
Abbreviations: CI = confidence interval; IQR = interquartile range; OR = odds ratio; RPLND = retroperitoneal lymph node dissection; SEER = Surveillance, Epidemiology, and End Results.
Multivariable analysis adjusted for race, age, RPLND, histologic type, and SEER stage.
For each 1-unit increase in SEER stage (localized to regional; regional to distant).
Multivariable analysis adjusted for percentage of foreign born, median family income, percentage with < 9th grade education, percentage without high school degree, percentage with more than a bachelor degree, percentage of families below the poverty line, percentage of unemployed, percentage of minority, and rural/urban status.
Discussion
The present analysis, to our knowledge, represents the first population-based study to analyze the outcomes of patients with UTM versus the outcomes of those with DTM. Patients with UTM were more frequently younger, were more diagnosed with a seminoma, and were more commonly not white. Although patients with UTM had comparable educational attainment, they were more often from counties with a greater number of foreign-born inhabitants. Patients with UTM also had poorer clinical stage disease than patients with DTM; however, cancer-specific mortality was comparable between the 2 groups, likely secondary to more patients with UTM having seminoma histologic features. Furthermore, the greater number of patients undergoing RPLND in the UTM cohort was likely secondary to the overall higher disease stage in those patients, although patients with UTM more commonly had the seminoma histologic type. Given that nonwhite race and living in a county with a greater number of foreign-born inhabitants was predictive of a UTM diagnosis, this disease entity might highlight a healthcare disparity not previously recognized.
Reports of malignancies in undescended testis have typically been confined to case series and case reports during the past 30 years.8–15 Omar et al13 reported one of the largest series to date (n = 12) of malignant tumors in undescended testes in patients who had presented with intra-abdominal and vague symptoms. They reported that 60% of these patients had the anaplastic variant of seminoma. Sham et al12 reported that in their experience of 40 patients with seminoma, 9 tumors were found in undescended testes. The most common presenting symptom in the undescended group was a painful groin mass or abdominal pain. In their study, for patients with DTM and UTM, after orchiectomy and radiotherapy (≥30 Gy to the pelvic and para-aortic lymph nodes for both groups), the 2-year survival was comparable for both groups for stage I and stage II malignancies (94% and 86%, respectively). Niang et al11 reported 5 cases of UTM in black Senegalese men. The mean age of these patients was 30 years; 3 patients had rupture of the tumor into the peritoneum, and the final pathologic examination demonstrated embryonal cancer in 3 and seminoma in 2.
A number of findings in this population-based analysis have been confirmed in previous reports. First, patients with UTM tend to be diagnosed more frequently with a seminoma histologic type.8,9,12,13,15 In the present study, we found that 71.0% of the patients with UTM were diagnosed with seminoma compared with 57.9% of the patients with DTM. Second, patients with UTM tended to be of a nonwhite race, similar to previous reports, which have discussed the diagnosis in black men of African descent and Asian descent (Japanese and Chinese).9,11,15 We found that on multivariable analysis, nonwhite race was independently associated with a diagnosis of UTM.
Recent studies have suggested that testicular cancer has become more significant (increasing incidence and mortality) in the minority and lower SES population.6,16–18 Richardson et al6 analyzed 46 studies conducted between 1966 and 2011 and found that SES had an inconclusive association with the development of testicular cancer. However, men living in lower SES geographic areas experienced poorer survival and greater mortality than their counterparts in higher SES areas.6 In addition, Dieckmann et al16 studied 180 men and found that lower levels of education were associated with a later-stage testicular cancer diagnosis and greater testicular cancer mortality. The SEER data from 2010 found that later-stage testicular cancer was diagnosed at greater rates in men from areas with greater poverty levels and lower educational attainment levels.5 According to a 2013 press release from the American Urological Association, Hispanic men experienced the largest annual percentage increase in the rate of a diagnosis of testicular cancer at 5.6% from 2002 to 2009.17 Furthermore, the data from the SEER database suggest that the incidence of testicular cancer among African-American men increased by 70.4% from 1973 to 2001.18
The increased incidence of testicular cancer in lower SES populations can be explained by the greater incidence of preterm births in this population. Although preterm births occur in 9.7% of all US singleton births, the rate for African-American men is double that of white men and is 25% greater for Hispanic men than for white men.19 The incidence of cryptorchidism is greater with preterm births than with full-term births, and the former might have a greater risk of testicular cancer. Furthermore, Abratt et al20 found that none of the black patients with germ cell tumors associated with cryptorchidism had undergone previous orchiopexy. Kokorowski et al21 reported that white non-Hispanic patients had a significantly increased likelihood of undergoing orchiopexy by 2 years of age compared with blacks or white/Hispanics. Although the utility and efficacy of screening for testicular cancer might be debateble,22 a possible explanation for this disparity is that men with less access to healthcare might not be diagnosed with a cryptorchid testis. These men might not be discovered and treated until advanced disease manifestations are present, consistent with the worse pathologic disease found in our study. This might indicate both a lack of education regarding testicular cancer and/or a lack of access to healthcare.
The present study had several limitations First, we were unable to assess whether patients had undergone previous orchiopexy for an undescended testis. This might have resulted in confounding because patients with DTM could have undergone a previous orchiopexy or could have been offered orchiopexy and did not undergo the procedure, leading to a subsequent diagnosis of UTM. Second, in the SEER database, information on the use of chemotherapy is lacking, which might have confounded the survival analysis between the 2 groups. Third, because the median age of diagnosis of UTM was 36 years, it is possible that the SES status had changed since birth. Fourth, the SES is measured in the SEER database at the county level, not than the individual level. Patients with a high SES status living in low SES counties (or vice versa) could have made the results less generalizable. Fifth, because of differences in the date of diagnosis and because the data covered an extended period (1988–2008), the estimates of survival outcomes could have been biased. Finally, most previous studies have addressed disparities in cancer related to lower SES assess, race, ethnicity, English as a second language, and lack of insurance, rather than foreign-born status, which has usually been implied.
Conclusion
The present study is the first population-based study to suggest that patients with UTM are more likely to be younger and nonwhite, to have a seminomatous histologic type and more advanced disease, and to be more commonly from regions with a greater proportion of foreign born persons compared with men diagnosed with DTM. Although the outcomes appeared to be similar to those for men with DTM, these results highlight an opportunity for clinicians to address a previously unrecognized healthcare disparity that might represent a lack of access to care and diagnosis for patients with UTM.
Clinical Practice Points.
Cryptorchidism is a common congenital anomaly, occurring in 1% to 4% of full-term and 1% to 45% of preterm infant males. Although the benefits of orchiopexy for cryptorchidism are clear, few reports have been published regarding the outcomes of patients who develop a malignancy in an undescended testis. Given the suggested SES disparities associated with cryptorchidism, we hypothesized that men presenting with a UTM would be of lower SES than were men with a DTM.
The significant factors associated with a UTM diagnosis included seminoma histologic features, RPLND, and SEER stage. The factors protective against a diagnosis of a UTM included white and Hispanic race. After adjusting for socioeconomic factors, residing in a county with more foreign-born inhabitants was associated with a diagnosis of UTM.
Although the outcomes appeared similar to those of men with a DTM, these results highlight an opportunity for clinicians to address a previously unrecognized healthcare disparity, which might represent a lack of access to care and diagnosis for patients with a UTM.
Footnotes
Disclosure
The authors have stated that they have no conflicts of interest.
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