Urinary TERT promoter mutations as non-invasive biomarkers for the comprehensive detection of urothelial cancerResearch in context
Patrice Hodonou Avogbe,
Arnaud Manel,
Emmanuel Vian,
Geoffroy Durand,
Nathalie Forey,
Catherine Voegele,
Maria Zvereva,
Md Ismail Hosen,
Sonia Meziani,
Berengere De Tilly,
Gilles Polo,
Olesia Lole,
Pauline Francois,
Tiffany Myriam Delhomme,
Christine Carreira,
Sara Monteiro-Reis,
Rui Henrique,
Behnoush Abedi-Ardekani,
Graham Byrnes,
Matthieu Foll,
Elisabete Weiderpass,
James McKay,
Carmen Jeronimo,
Ghislaine Scelo,
Florence Le Calvez-Kelm
Affiliations
Patrice Hodonou Avogbe
International Agency for Research on Cancer (IARC), Lyon, France
Arnaud Manel
Protestant Clinic of Lyon, Urology department, Lyon, France
Emmanuel Vian
Protestant Clinic of Lyon, Urology department, Lyon, France
Geoffroy Durand
International Agency for Research on Cancer (IARC), Lyon, France
Nathalie Forey
International Agency for Research on Cancer (IARC), Lyon, France
Catherine Voegele
International Agency for Research on Cancer (IARC), Lyon, France
Maria Zvereva
International Agency for Research on Cancer (IARC), Lyon, France; Faculty of Chemistry, Lomonosov Moscow State University, Moscow, Russia
Md Ismail Hosen
International Agency for Research on Cancer (IARC), Lyon, France
Sonia Meziani
International Agency for Research on Cancer (IARC), Lyon, France
Berengere De Tilly
Protestant Clinic of Lyon, Urology department, Lyon, France
Gilles Polo
Protestant Clinic of Lyon, Urology department, Lyon, France
Olesia Lole
International Agency for Research on Cancer (IARC), Lyon, France
Pauline Francois
International Agency for Research on Cancer (IARC), Lyon, France
Tiffany Myriam Delhomme
International Agency for Research on Cancer (IARC), Lyon, France
Christine Carreira
International Agency for Research on Cancer (IARC), Lyon, France
Sara Monteiro-Reis
Portuguese Oncology Institute of Porto, Research Center (CI-IPOP), Porto, Portugal
Rui Henrique
Portuguese Oncology Institute of Porto, Research Center (CI-IPOP), Porto, Portugal; Portuguese Oncology Institute of Porto (IPOP), Department of Pathology, Porto, Portugal; Institute of Biomedical Sciences Abel Salazar, University of Porto (ICBAS-UP), Porto, Portugal
Behnoush Abedi-Ardekani
International Agency for Research on Cancer (IARC), Lyon, France
Graham Byrnes
International Agency for Research on Cancer (IARC), Lyon, France
Matthieu Foll
International Agency for Research on Cancer (IARC), Lyon, France
Elisabete Weiderpass
International Agency for Research on Cancer (IARC), Lyon, France
James McKay
International Agency for Research on Cancer (IARC), Lyon, France
Carmen Jeronimo
Portuguese Oncology Institute of Porto, Research Center (CI-IPOP), Porto, Portugal; Portuguese Oncology Institute of Porto (IPOP), Department of Pathology, Porto, Portugal; Institute of Biomedical Sciences Abel Salazar, University of Porto (ICBAS-UP), Porto, Portugal
Ghislaine Scelo
International Agency for Research on Cancer (IARC), Lyon, France
Florence Le Calvez-Kelm
International Agency for Research on Cancer (IARC), Lyon, France; Corresponding author at: International Agency for Research on Cancer, Genetic Cancer Susceptibility group, 150 Cours Albert Thomas, 69372 Lyon Cedex 08, France.
Background: Recurrent mutations in the promoter of the telomerase reverse transcriptase (TERT) gene (C228T and C250T) detected in tumours and cells shed into urine of urothelial cancer (UC) patients are putative biomarkers for UC detection and monitoring. However, the possibility of detecting these mutations in cell-free circulating DNA (cfDNA) in blood and urine, or DNA from urinary exfoliated cells (cellDNA) with a single-gene sensitive assay has never been tested in a case-control setting. Methods: We developed a single-plex assay (UroMuTERT) for the detection of low-abundance TERT promoter mutations. We tested 93 primary and recurrent UC cases and 94 controls recruited in France (blood, urine samples and tumours for the cases), and 50 primary UC cases and 50 controls recruited in Portugal (urinary exfoliated cell samples). We compared our assay with urine cytology. Findings: In the French series, C228T or C250T were detected in urinary cfDNA or cellDNA in 81 cases (87·1%; 95% CI 78·6–93·2), and five controls (Specificity 94·7%; 95%CI 88·0–98·3), with 98·6% (95% CI 92·5–99·96) concordance in matched tumours. Detection rate in plasma cfDNA among cases was 7·1%. The UroMuTERT sensitivity was (i) highest for urinary cfDNA and cellDNA combined, (ii) consistent across primary and recurrent cases, tumour stages and grades, (iii) higher for low-risk non-muscle invasive UC (86·1%) than urine cytology (23·0%) (P < 0·0001) and (iv) 93·9% when combined with cytology. In the Portuguese series – the sensitivity and specificity for detection of UC with urinary cellDNA was 68·0% (95% CI 53·3–80·5) and 98·0% (95% CI 89·3–100·0). Interpretation: TERT promoter mutations detected by the UroMuTERT assay in urinary DNA (cfDNA or cellDNA) show excellent sensitivity and specificity for the detection of UC, significantly outperforming that of urine cytology notably for detection of low-grade early stages UC. Fund: French Cancer League; French Foster Research in Molecular Biology and European Commission FP7 Marie Curie COFUND. Keywords: Urine, Blood, Cell DNA, Cell-free DNA, TERT mutations, Urothelial cancer detection