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American Journal of Epidemiology Advance Access originally published online on April 11, 2008
American Journal of Epidemiology 2008 167(12):1438-1445; doi:10.1093/aje/kwn080
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American Journal of Epidemiology Published by the Johns Hopkins Bloomberg School of Public Health 2008.

ORIGINAL CONTRIBUTIONS

Insulin-like Growth Factor 1, Insulin-like Growth Factor-Binding Protein 3, and Testicular Germ-Cell Tumor Risk

Victoria M. Chia1, Sabah M. Quraishi1, Barry I. Graubard1, Mark V. Rubertone2, Ralph L. Erickson3, Frank Z. Stanczyk4 and Katherine A. McGlynn1

1 Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD
2 US Army Center for Health Promotion and Preventive Medicine, Washington, DC
3 Walter Reed Army Institute of Research, Forest Glen, MD
4 Keck School of Medicine, University of Southern California, Los Angeles, CA

Correspondence to Dr. Victoria M. Chia, Hormonal and Reproductive Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Executive Plaza South, Suite 550, 6120 Executive Boulevard, Rockville, MD 20892-7234 (e-mail: chiav{at}mail.nih.gov).

Received for publication November 6, 2007. Accepted for publication March 11, 2008.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Studies have consistently shown that taller men are at increased risk of testicular germ-cell tumors. Thus, it is plausible that factors associated with height may also influence risk of these tumors. The authors examined associations between testicular germ-cell tumor risk and circulating concentrations of insulin-like growth factor 1 (IGF-1) and insulin-like growth factor-binding protein 3 (IGFBP-3) among 517 cases and 790 controls from the US Servicemen's Testicular Tumor Environmental and Endocrine Determinants (STEED) Study (2002–2005). Odds ratios and 95% confidence intervals were estimated using logistic regression models, adjusting for age, race/ethnicity, height, and body mass index. All tests of significance were two-sided. Overall, there were no associations between IGF-1 or IGFBP-3 concentrations and risk of testicular germ-cell tumors (p > 0.05). However, when cases were separated by histologic type, there was a suggestion of a reduction in seminoma risk associated with the highest concentrations of IGF-1 as compared with the lowest concentrations (odds ratio = 0.66, 95% confidence interval: 0.40, 1.09). Although there were no overall associations with insulin-like growth factor, contrary to expectation, there was a suggestion that IGF-1 concentrations may be inversely associated with risk of seminoma.

hormones; insulin-like growth factor binding protein 3; insulin-like growth factor I; testicular neoplasms

Abbreviations: IGF, insulin-like growth factor; IGFBP-3, insulin-like growth factor-binding protein 3; STEED, US Servicemen's Testicular Tumor Environmental and Endocrine Determinants


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Testicular germ-cell tumors are the most common tumors among American men aged 15–35 years. However, other than cryptorchidism, family history of testicular cancer, and prior diagnosis of testicular germ-cell tumors, risk factors have not been well-identified (1, 2). A number of studies have reported that increased adult height may be a risk factor for testicular germ-cell tumors (3–10), thereby suggesting that factors related to adult height may also be related to risk of these tumors. One such height-related factor may be insulin-like growth factor (IGF) and the IGF pathway (11).

The IGF pathway, which contributes to a spectrum of regulatory processes, including somatic growth and cellular proliferation, includes two ligand proteins (IGF-1 and IGF-2), their receptors, and six binding proteins (12). IGF-1 has been shown to be a potent mitogen that initiates signaling cascades via binding to its receptor (13, 14). IGF-1 may also have antiapoptotic properties (15). Bioavailable concentrations of IGF-1 are primarily determined by its affinity for its binding proteins, of which insulin-like growth factor-binding protein 3 (IGFBP-3) sequesters approximately 80 percent (12). Although increased IGF-1 concentrations have been reported to be positively associated with prostate cancer, colon cancer, and premenopausal breast cancer (16), no studies published to date (to our knowledge) have assessed whether IGF-1 and IGFBP-3 concentrations are associated with risk of testicular germ-cell tumors. Therefore, we conducted a case-control analysis to determine the association between IGF-1 and IGFBP-3 concentrations and risk of testicular germ-cell tumors.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Study population
Study participants, enrolled in the US Servicemen's Testicular Tumor Environmental and Endocrine Determinants (STEED) Study between April 2002 and January 2005, have been previously described in detail (3). Briefly, all men who had at least one serum sample stored in the Department of Defense Serum Repository (Silver Spring, Maryland) and were younger than 45 years of age were eligible for the study. Men who developed testicular germ-cell tumors while on active duty were eligible to be enrolled as cases if they were diagnosed at a date later than the date of serum donation. Diagnoses of testicular germ-cell tumors were limited to classic seminomas or nonseminomas. Men who developed spermatocytic seminomas were not eligible for inclusion. Eligible controls, men who did not develop testicular germ-cell tumors, were pair-matched to cases on the basis of age (<1 year), race/ethnicity (White, Black, other), and date of serum sample donation (<30 days). Of the eligible cases (n = 853) and controls (n = 1,182), 767 cases (90 percent) and 928 controls (79 percent) agreed to participate and completed the study. Written, informed consent was obtained from all participants, and the study was approved by the institutional review boards of the National Cancer Institute and the Walter Reed Army Institute of Research.

Each participant completed a study questionnaire through a computer-assisted telephone interview. Questionnaires elicited information on demographic factors, such as height and weight, and on known or suspected risk factors for testicular germ-cell tumors. For cases, the reference date was the date of tumor diagnosis. For controls, the reference date was the tumor diagnosis date of the matched case. The median time from serum blood collection to diagnosis date was 4.4 years, ranging from 15 days to 13.3 years; however, only 16 participants had blood drawn less than 1 year prior to the date of diagnosis.

Measurement of IGF-1 and IGFBP-3 concentrations
IGF-1 and IGFBP-3 were quantified via chemiluminescence immunoassay using the IMMULITE analyzer (Siemens Medical Solutions Diagnostics, Los Angeles, California). The sensitivities of the assays were 20 ng/ml for IGF-1 and 0.1 µg/ml for IGFBP-3. Three control samples were included on each plate; interassay coefficients of variation for IGF-1 and IGFBP-3 were 4.7 percent and 8.8 percent, respectively.

Statistical analysis
Questionnaire data and serum samples were available for analysis from 517 cases and 790 controls. Concentrations of IGF-1 and IGFBP-3 followed a normal distribution and were not log-transformed. Concentrations were then divided into quartiles based on the cutpoints in controls. The molar ratio of IGF-1 to IGFBP-3 (IGF molar ratio), often used as an estimate of free IGF-1 concentration, was calculated as [IGF-1 (ng/ml) x 0.130]/[IGFBP-3 (ng/ml) x 0.036]. The reference group for analyses was the lowest quartile.

Correlations between circulating concentrations of IGF-1 and IGFBP-3 were assessed using Spearman's correlation coefficient. Generalized linear models, adjusting for age, race/ethnicity (White, Black, other), and date of serum donation, were used to assess associations between selected characteristics, including age, adult height (in cm), adult weight (in kg), body mass index (weight (kg)/height (m)2), and IGF concentrations in controls. Student's t tests were used to compare mean IGF concentrations between cases and controls and between seminomas and nonseminomas.

Logistic regression models, adjusting for age, race/ethnicity, serum donation date, body mass index, and adult height, were used to estimate odds ratios and 95 percent confidence intervals for associations between IGF concentrations and testicular germ-cell tumor risk, overall and by histologic type. Conditional logistic regression models, adjusting for the matched sets, were also examined. Tests for trend were evaluated by including the IGF categories as continuous ordinal variables in the regression model. Differences between histologic types were assessed by including only the two case groups in the outcome variable. Effect modification by adult height was examined, with additional exploratory analyses stratified by adult weight, body mass index, and length at birth—other risk factors that may be associated with IGF concentrations. Adult height, adult weight, body mass index, and length at birth were dichotomized at the median cutpoint in controls. Interactions were evaluated by including a multiplicative variable between a dichotomous effect modifier and a continuous IGF concentration variable. All statistical analyses were performed using SAS, version 9.1 (SAS Institute, Cary, North Carolina). All tests of significance were two-sided, and p values less than 0.05 were considered statistically significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Selected characteristics of cases and controls are presented in table 1. Cases and controls had a mean age of 28 years. Approximately 85 percent of participants were White. Compared with controls, cases had statistically significantly higher frequencies of prior cryptorchidism (p < 0.01) and family history of testicular cancer (p = 0.01). Cases were statistically significantly taller than controls (179.4 cm vs. 178.3 cm; p < 0.01) but did not differ in weight (p = 0.14) or body mass index (p = 0.36).


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  		TABLE 1. Characteristics of participants in a case-control study of insulin-like growth factors and testicular germ-cell tumors, US Servicemen's Testicular Tumor Environmental and Endocrine Determinants Study, 2002–2005

 
Among controls, when IGFs were examined as continuous variables, the r values for correlations between height (cm) and IGF-1 and IGFBP-3 concentrations were 0.11 (p = 0.003) and 0.09 (p = 0.008), respectively. Only IGFBP-3 concentrations were statistically significantly correlated with weight (r = 0.16, p < 0.0001) and body mass index (r = 0.11, p = 0.002). When we examined IGF concentrations in categories of age, height, weight, and body mass index (table 2), IGF-1, IGFBP-3, and their molar ratio were all inversely associated with age (trend p's < 0.01). Only IGF-1 concentrations were positively associated with quartiles of height (p-trend = 0.03). Both IGF-1 and IGFBP-3 concentrations were statistically significantly and positively associated with increasing quartiles of weight and body mass index.


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  		TABLE 2. Mean* concentrations of insulin-like growth factors among controls, by selected characteristics, US Servicemen's Testicular Tumor Environmental and Endocrine Determinants Study, 2002–2005

 
Mean concentrations of IGF-1 and IGFBP-3 and the IGF molar ratio are presented in table 3. There were statistically significant correlations between IGF-1 and IGFBP-3 among controls (r = 0.58). When the cases were separated by histologic type, mean IGF-1 and IGFBP-3 concentrations were statistically significantly lower in men with seminomas than in men with nonseminomas (p < 0.01 for IGF-1 and p = 0.01 for IGFBP-3).


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  		TABLE 3. Mean concentrations of insulin-like growth factors among testicular germ-cell tumor cases and controls, US Servicemen's Testicular Tumor Environmental and Endocrine Determinants Study, 2002–2005

 
There were no associations between IGF-1 and IGFBP-3 concentrations and overall risk of testicular germ-cell tumors (table 4). However, when cases were separated by histologic type, there was a suggestion that seminoma cases with the highest IGF-1 concentrations had a 34 percent reduction in risk compared with those with the lowest concentrations (odds ratio = 0.66, 95 percent confidence interval: 0.40, 1.09). Additional adjustment for IGFBP-3 showed similar results. For men with nonseminomas, there was no reduction in risk associated with IGF-1 concentrations; these trends, compared with those for seminomas, were statistically significant (p = 0.04). IGFBP-3 concentrations were not associated with testicular germ-cell tumors overall or with either seminomas or nonseminomas. Similarly, no associations were seen when IGFBP-3 concentration was adjusted for IGF-1. Results of the analyses using conditional logistic regression models did not differ from the results of the unconditional models (data not shown).


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  		TABLE 4. Odds of testicular germ-cell tumors associated with insulin-like growth factors, US Servicemen's Testicular Tumor Environmental and Endocrine Determinants Study, 2002–2005

 
As table 5 shows, there were suggestions of differences in the seminoma risk associated with IGF molar ratio by height. For seminoma cases with heights less than 177.8 cm, the median cutpoint in controls, there was a suggestion of a reduction in risk associated with increasing IGF molar ratio (p = 0.06). In contrast, for seminoma cases with heights greater than or equal to 177.8 cm, there was no reduction in risk (p = 0.75). These differences were not statistically significant, however (interaction p's > 0.05). Similar results were seen when data were stratified by weight and body mass index at the median value (data not shown). No differences in associations were seen when results were stratified by length at birth (data not shown).


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  		TABLE 5. Odds of testicular germ-cell tumors associated with insulin-like growth factors, according to height, US Servicemen's Testicular Tumor Environmental and Endocrine Determinants Study, 2002–2005

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
In the current study, although there were no overall associations between serum IGF concentrations and risk of testicular germ-cell tumors, a reduction in seminoma risk associated with the highest IGF-1 concentrations was suggested. There were no associations with nonseminoma risk. When results were stratified by adult height and body mass index, there were suggestions of differences in seminoma risk associated with IGF molar ratio, with reductions in risk being apparent only in the men who were shorter or had a lower body mass index.

It has been hypothesized that risk of testicular germ-cell tumors may be associated with alterations in the IGF pathway (11) because of the reported associations between greater adult height and increased risk of these tumors (3–10). As was previously reported in the STEED Study (3), there was a statistically significant increased risk of testicular germ-cell tumors associated with greater height, and this association was particularly evident in men with seminomas. When we examined relations between serum IGF concentration and height in the current analysis, increased serum IGF-1 concentrations were associated with increased height, an association that has also been observed in other studies (17, 18). Further evidence in support of an IGF-1-seminoma relation includes the observation that although IGF-1 mRNA expression does not differ between normal testicular tissue and seminomas, several of the IGF binding proteins are down-regulated in seminomas as compared with normal testicular tissue (19), thus allowing increased concentrations of free IGF-1. These findings may not have been present in our study, because there may have been differences in both concentrations and actions of IGFs in blood versus tissue.

Positive associations between serum IGF-1 concentration and risks of premenopausal breast (16, 20), prostate (16), and colon (21) cancer have been observed. We did not find a similar association with risk of testicular germ-cell tumors in the current study. IGF-1 concentrations were associated with seminoma, but the association was inverse of that seen with other cancers. When results were further stratified by height, the suggested inverse association appeared to be stronger in shorter men.

One possible mechanism for the unexpected inverse association may operate through the relations of perinatal factors with IGFs and testicular germ-cell tumor risk. Low birth weight and being born small for gestational age have been associated with increased risk of testicular germ-cell tumors in some studies (22–24). Because these measures of smaller birth size are also associated with both shorter childhood stature (25, 26) and shorter adult stature (27) and with lower IGF-1 concentrations (28, 29), it could be expected that an increased risk of testicular germ-cell tumors may be associated with lower IGF-1 concentrations in early life. This could be an explanation for the observations in shorter men, whereas in taller men, the increased risk of testicular germ-cell tumors could be due to mechanisms other than the IGF pathway. It is uncertain, however, how IGF concentrations change over time within individuals and whether lower perinatal concentrations necessarily reflect lower concentrations in adults. It is also unclear whether there is a correlation between perinatal IGF-1 concentrations and adult height.

Additionally, an observation that serum testosterone concentrations are highly correlated with IGF molar ratio (r = 0.76, p < 0.001) in boys further complicates these relations (30). Few, if any, studies have assessed the associations between androgen concentrations and risk of testicular germ-cell tumors; however, it has been posited that differences in risk between seminomas and nonseminomas may be due to androgen sensitivity, with higher androgen sensitivity leading to seminomas and lower androgen sensitivity leading to nonseminomas (31).

Because height has been shown to be associated with risk of both seminomas and nonseminomas (3, 4, 6), suggestions of seminoma associations with IGF-1 may be independent of height. There may be other explanations for the relation between height and testicular germ-cell tumor risk, including exposures such as childhood nutrition; however, one study that examined this relation did not find any associations with childhood dairy intake (3). Thus, the relations among height, IGFs, and risk of testicular germ-cell tumors are likely to be complex and may not be easily explained.

Strengths of this study include the fact that it was one of the largest case-control investigations of testicular cancer to be drawn from a well-defined population (military servicemen) and that we had access to serum samples collected prior to tumor diagnosis. Although all serum samples were collected prior to diagnosis of testicular germ-cell tumors, we performed sensitivity analyses to test whether there were differences in risk estimates when serum samples taken within 1, 2, or 3 years of diagnosis were excluded. Excluding these samples did not significantly alter the risk estimates. Although studies have shown absolute differences in circulating IGF concentrations by type of assay used, correlations of concentrations between assays have been high, ranging from 0.90 to 0.98 (32–35). Even though there are differences in absolute concentrations between assays, we feel confident that the relative comparisons are valid. Additional strengths of this study include the facts that histologic data were incorporated and that all diagnoses were confirmed. However, despite the large sample size, we had limited statistical power to assess associations within strata of histology and height, and differences between strata may have been due to chance. In addition, a large number of comparisons were made, which also increased the chance of borderline statistically significant findings.

In conclusion, although we observed no overall associations with IGF in this study, there was a suggestion of a reduction in seminoma risk associated with high IGF-1 concentrations, particularly among shorter men. Differences in risk by histologic type are provocative and may give insight into differences in risk factors between seminomas and nonseminomas. Replication of these results in other populations would be beneficial, as would additional investigations of differences between seminomas and nonseminomas and of IGFs and other hormones associated with height and testicular germ-cell tumors.


   ACKNOWLEDGMENTS
 
This work was supported by the Intramural Research Program of the National Institutes of Health, National Cancer Institute.

The authors thank Emily Steplowski of Information Management Services, Inc. (Rockville, Maryland) for her contributions to data management.

The opinions or assertions contained herein are the private views of the authors and are not to be construed as official or as reflecting the views of the Department of the Army or the Department of Defense.

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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