<table><caption>TABLE 5 (Continued)</caption><thead><tr><th rowspan="2"></th><th colspan="3">Non-seminomas</th><th colspan="3">Seminomas</th><th rowspan="2">P-HET**</th></tr><tr><th>N cases/<br/>N controls</th><th>Crude OR<br/>(95% CI)</th><th>Adjusted<br/>OR*<br/>(95% CI)</th><th>N cases/<br/>N controls</th><th>Crude OR<br/>(95% CI)</th><th>Adjusted<br/>OR*<br/>(95% CI)</th></tr></thead><tbody><tr><td>Activities for human health (85.1)</td><td>10/62</td><td>0.62 (0.30–1.27)</td><td>0.66 (0.32–1.36)</td><td>16/62</td><td>0.84 (0.47–1.52)</td><td>0.82 (0.45–1.51)</td><td>0.64</td></tr><tr><td>Hospital activities (85.1A)</td><td>7/36</td><td>0.63 (0.26–1.54)</td><td>0.67 (0.27–1.63)</td><td>12/36</td><td>1.16 (0.58–2.35)</td><td>1.10 (0.53–2.28)</td><td>0.39</td></tr><tr><td>Social work activities (85.3)</td><td>5/16</td><td>0.88 (0.30–2.58)</td><td>0.93 (0.32–2.72)</td><td>5/16</td><td>1.22 (0.43–3.46)</td><td>1.12 (0.38–3.32)</td><td>0.81</td></tr></tbody></table>

Significant differences in bold.

to a lack of power and concerns of potential recall bias when limiting the analyses to cases and controls with participating mothers. To limit recall and social desirability bias, cases and controls, as well as the subjects' mothers, were given a document to prepare for the telephone interview regarding their professional and residential history and were invited to bring their health records to the interview. Yet, we cannot exclude that social desirability bias may apply to responses to items such as fertility, medical history, smoking, alcohol consumption, and substance use, which constitutes a limitation in the present study (79–82). Pre- and perinatal factors of participants and the socio-economic status of mothers at birth were similar between the groups of subjects with interviewed and non-interviewed mothers (48). We used the subsample of participants with interviewed mothers to study the agreement between the occupational data collected from the sons and from their mothers. Because of the good agreement, it appeared justified to take into account the sons' data and thus double the number of participants, increasing the power of our study (83). The analysis of parental jobs at birth reported by the mothers showed only one association consistent with the results on the ISCO-68 and NAF-1999 codes of the sons' data. Categories that appeared to be associated with the main analyses or from the mothers' data could not be confirmed in the other analysis because of an insufficient number of subjects, whether the data came from participants or mothers. However, the positive association observed after adjustment from the mothers' data for paternal jobs or industries “Crops” seems to be—focusing on the field of activity—in accordance with “Specialised farmers” found significant from the sons' data.

To observe the relationship between parental jobs at birth and TGCT in offspring, the use of two nomenclatures based on job and industry categories and subcategories appeared complementary but involved multiple analyses. This limitation has been previously discussed (65). Although our results may be interpreted with caution, overall they appear to be consistent with the literature.

Endocrine disruptors are likely to be involved in the development of TGCTs (15, 20, 22). Due to their toxicological characteristics, including low-dose effects, non-monotonic dose-effect relationships, and sensitivity to the cocktail effect (22, 23), we cannot exclude that other environmental, domestic, or even occupational exposures, whether these exposures are concomitant or not, depending on half-lives or delayed effects, may participate in the development of TGCT in the offspring through additive or synergistic relationship with the occupational exposures appearing to be associated with TGCT here (15, 22, 23). However, a recent meta-analysis studying the link between exposure to EDC and the risk of TGCT highlighted that maternal, but not postnatal adult male, EDC exposures were consistently associated with a higher risk of TGCT, particularly of non-seminomas (22), which confirms the relevance of our study and our results. Furthermore, the assessment of cocktail effects and

their involvement in health issues remains a methodological challenge (84, 85), which is reflected in the fact that this meta-analysis was unable to identify any study looking at mixtures of substances (22). Identifying jobs possibly involved in TGCT development could be an opportunity to assess the link between global human exposures in real situations, rather than individual compounds. Birth was chosen as the period of parental occupational exposure of interest, being a proxy of periconceptional, gestational, and first 1,000 days of life exposures, key periods in child development, assuming, on the basis of employment data at the time of the birth, that the parents remain in the same job or field of activity overall (86). This could be a preliminary work to identify exposures at risk in the early childhood period, which could be completed later by studies on each of these periods independently.

## 5 Conclusion

Our study suggests that parental jobs or industries in perinatal life, such as paternal jobs at birth as a service worker, protective service worker, transport equipment operator, specialized farmer, and maternal jobs as secondary education teachers or working in secondary education at birth, may be related to the development of adult TGCT in their sons, which appears consistent with some previous studies, with specific features depending on the histological type.

Further studies on the different occupational exposures related to these jobs and industries of the parents at birth are needed, as we have done or plan to do with solvents, pesticides, or heavy metals (87). In addition, the combined effect of early life exposure, leading to the development of GCNIS, and later life exposure in adolescence or adulthood, acting as a trigger for the evolution of GCNIS to TGCT, should be taken into account in future studies.

## Data availability statement

The datasets presented in this article are not readily available because data are available on reasonable request. The data collection process is described in the method section of this article. Requests to access the datasets should be directed to BF beatrice.fervers@lyon.unicancer.fr.

## Ethics statement

The studies involving humans were approved by the French Ethics Committee (ref. no. A14-94), the French National Agency for the

<footnote>*Adjusted for sibship size, born from multiple pregnancies, personal history of testicular trauma, family history of testicular cancer, and family history of cryptorchidism.</footnote>

<footnote>**p-value for heterogeneity derived from the likelihood ratio test, comparing seminoma versus non-seminoma tumours in adjusted models.</footnote>
Safety of Medicines and Health Products (ref. no. 140184B-12), and the IARC Ethics Committee (ref. no. 14–26) and declared to the Commission nationale de l'Informatique et des Libertés (MR-001, ref. no. 2016–177). The studies were conducted in accordance with the local legislation and institutional requirements. The participants provided their written informed consent to participate in this study.

## Author contributions

AP: Conceptualization, Formal analysis, Funding acquisition, Methodology, Writing – original draft, Writing – review & editing. AD: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Writing – review & editing. FD: Data curation, Software, Writing – review & editing. MG: Validation, Writing – review & editing. AC: Project administration, Validation, Writing – review & editing. ML: Data curation, Formal analysis, Software, Writing – review & editing. BD: Data curation, Writing – review & editing. HK: Investigation, Methodology, Resources, Validation, Writing – review & editing. JHS: Methodology, Supervision, Writing – review & editing. RB: Data curation, Validation, Writing – review & editing. OP: Funding acquisition, Project administration, Writing – review & editing. HB: Data curation, Resources, Writing – review & editing. CH: Resources, Writing – review & editing. VL-C: Resources, Writing – review & editing. SV: Resources, Writing – review & editing. LB: Resources, Writing – review & editing. AO: Conceptualization, Methodology, Supervision, Validation, Writing – review & editing. JAS: Conceptualization, Methodology, Supervision, Validation, Writing – review & editing. BF: Conceptualization, Funding acquisition, Investigation, Methodology, Project administration, Supervision, Validation, Writing – review & editing. BC: Conceptualization, Investigation, Methodology, Supervision, Validation, Writing – review & editing.

## Collaborators

TESTIS Study Group: Aude Fléchon and Elodie Belladame (Centre Léon Bérard, Lyon). Véronique Drouineaud, Céline Chalas, Aurélie Vincent, Anne-Sophie Gille, Laurianne Kremer, Myriam Virlouvet, Lucile Ferreux, Guillemette Perier, Pauline Peretout, and Diane Rivet (Cochin Hospital, Paris); Rachel Levy and Isabelle Berthaut (Tenon Hospital, Paris); Florence Eustache, Nathalie Sermonande, Marine Durand, and Charlène Harbemont (Jean Verdier Hospital, Paris); Jeanne Perrin, Jacqueline Saias-Magnan, Carole Daoud-Deveze, and Catherine Metzler-Guillemain (La Conception Hospital, Marseille); Myriam Daudin and François Isus (Paule de Viguier Hospital, Toulouse); Florence Brugnon, Valérie Bruhat, and Cyril Bouche (Estaing Hospital, Clermont-Ferrand); Isabelle Koscinski, Cécile Greze, Françoise Schmitt, Marius Teletin, and Nathalie Guyomard (Obstetric Medico-Surgical Centre, Strasbourg); Aline Papaxanthos, Volcy Soula, and Lucie Chansel (Pellegrin maternity Hospital, Bordeaux); Sandrine Giscard d'Estaing, Pascale Dehee, and Delphine Yalcinkaya (Femme-Mère-Enfant Hospital, Lyon); Céline Bouillon, Cynthia Frapsauce, Anne Viallon, and Catherine Guerin (Bretonneau Hospital, Tour); Berengere Ducrocq and Florian Dossou Gbete (Calmette Hospital, Lille); Marie-Ange Clarotti, Amélie Ancelle, and Emeline Bovet-Courtois (Caen Hospital, Caen); Oxana Blagosklonov and Séverine Bey (Jean Minjoz Hospital,

Besançon); Célia Ravel, Guilhem Jouve, Laurent Vandenbroucke, and Agnès Letremy (South Hospital, Rennes); Patricia Fauque, Julie Barberet, and Céline Bruno (Dijon Hospital, Dijon); Stéphanie Lattes Emmanuelle Thibault, Pierre Besnier, and Adrien Perche (l'Archet Hospital, Nice); Catherine Diligent (Regional University Maternity Hospital, Nancy); Anna Gala and Christelle Saintpeyre (Arnaud de Villeneuve Hospital, Montpellier); Sylvianne Hennebicq and Julien Bessonnat (Couple-Enfant Hospital, Grenoble); Marie-Claude Blocquaux (Maison Blanche Hospital, Reims).

## Funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. The project was supported by funding from the French National Cancer Institute (INCa, N°2013-721 143) and the Institut National de la Santé et de la Recherche Médicale (Inserm, N°ENV201306/CLB). The TESTIS-PRO project was supported by funding from the Fondation de France. We gratefully acknowledge the participants and their mothers for providing data and the medical practitioners for providing pathology reports.

## Acknowledgments

We acknowledge the Direction de la Recherche Clinique from the Toulouse University Hospital for their contribution to the coordination of the investigation centres. We thank the IPSOS Company for conducting telephone interviews.

## Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

The reviewer CC declared a past co-authorship with the authors to the handling editor.

The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.

## Publisher's note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

## Supplementary material

The Supplementary material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fpubh.2023.1303998/full#supplementary-material
Safety of Medicines and Health Products (ref. no. 140184B-12), and the IARC Ethics Committee (ref. no. 14–26) and declared to the Commission nationale de l'Informatique et des Libertés (MR-001, ref. no. 2016–177). The studies were conducted in accordance with the local legislation and institutional requirements. The participants provided their written informed consent to participate in this study.

## Author contributions

AP: Conceptualization, Formal analysis, Funding acquisition, Methodology, Writing – original draft, Writing – review & editing. AD: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Writing – review & editing. FD: Data curation, Software, Writing – review & editing. MG: Validation, Writing – review & editing. AC: Project administration, Validation, Writing – review & editing. ML: Data curation, Formal analysis, Software, Writing – review & editing. BD: Data curation, Writing – review & editing. HK: Investigation, Methodology, Resources, Validation, Writing – review & editing. JHS: Methodology, Supervision, Writing – review & editing. RB: Data curation, Validation, Writing – review & editing. OP: Funding acquisition, Project administration, Writing – review & editing. HB: Data curation, Resources, Writing – review & editing. CH: Resources, Writing – review & editing. VL-C: Resources, Writing – review & editing. SV: Resources, Writing – review & editing. LB: Resources, Writing – review & editing. AO: Conceptualization, Methodology, Supervision, Validation, Writing – review & editing. JAS: Conceptualization, Methodology, Supervision, Validation, Writing – review & editing. BF: Conceptualization, Funding acquisition, Investigation, Methodology, Project administration, Supervision, Validation, Writing – review & editing. BC: Conceptualization, Investigation, Methodology, Supervision, Validation, Writing – review & editing.

## Collaborators

TESTIS Study Group: Aude Fléchon and Elodie Belladame (Centre Léon Bérard, Lyon). Véronique Drouineaud, Céline Chalas, Aurélie Vincent, Anne-Sophie Gille, Laurianne Kremer, Myriam Virlouvet, Lucile Ferreux, Guillemette Perier, Pauline Peretout, and Diane Rivet (Cochin Hospital, Paris); Rachel Levy and Isabelle Berthaut (Tenon Hospital, Paris); Florence Eustache, Nathalie Sermonande, Marine Durand, and Charlène Harbemont (Jean Verdier Hospital, Paris); Jeanne Perrin, Jacqueline Saias-Magnan, Carole Daoud-Deveze, and Catherine Metzler-Guillemain (La Conception Hospital, Marseille); Myriam Daudin and François Isus (Paule de Viguier Hospital, Toulouse); Florence Brugnon, Valérie Bruhat, and Cyril Bouche (Estaing Hospital, Clermont-Ferrand); Isabelle Koscinski, Cécile Greze, Françoise Schmitt, Marius Teletin, and Nathalie Guyomard (Obstetric Medico-Surgical Centre, Strasbourg); Aline Papaxanthos, Volcy Soula, and Lucie Chansel (Pellegrin maternity Hospital, Bordeaux); Sandrine Giscard d'Estaing, Pascale Dehee, and Delphine Yalcinkaya (Femme-Mère-Enfant Hospital, Lyon); Céline Bouillon, Cynthia Frapsauce, Anne Viallon, and Catherine Guerin (Bretonneau Hospital, Tour); Berengere Ducrocq and Florian Dossou Gbete (Calmette Hospital, Lille); Marie-Ange Clarotti, Amélie Ancelle, and Emeline Bovet-Courtois (Caen Hospital, Caen); Oxana Blagosklonov and Séverine Bey (Jean Minjoz Hospital,

Besançon); Célia Ravel, Guilhem Jouve, Laurent Vandenbroucke, and Agnès Letremy (South Hospital, Rennes); Patricia Fauque, Julie Barberet, and Céline Bruno (Dijon Hospital, Dijon); Stéphanie Lattes Emmanuelle Thibault, Pierre Besnier, and Adrien Perche (l'Archet Hospital, Nice); Catherine Diligent (Regional University Maternity Hospital, Nancy); Anna Gala and Christelle Saintpeyre (Arnaud de Villeneuve Hospital, Montpellier); Sylvianne Hennebicq and Julien Bessonnat (Couple-Enfant Hospital, Grenoble); Marie-Claude Blocquaux (Maison Blanche Hospital, Reims).

## Funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. The project was supported by funding from the French National Cancer Institute (INCa, N°2013-721 143) and the Institut National de la Santé et de la Recherche Médicale (Inserm, N°ENV201306/CLB). The TESTIS-PRO project was supported by funding from the Fondation de France. We gratefully acknowledge the participants and their mothers for providing data and the medical practitioners for providing pathology reports.

## Acknowledgments

We acknowledge the Direction de la Recherche Clinique from the Toulouse University Hospital for their contribution to the coordination of the investigation centres. We thank the IPSOS Company for conducting telephone interviews.

## Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

The reviewer CC declared a past co-authorship with the authors to the handling editor.

The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.

## Publisher's note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

## Supplementary material

The Supplementary material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fpubh.2023.1303998/full#supplementary-material
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