Activating mutations of genes in the PI3K/AKT/mTOR signaling pathway and ovarian reserve status in patients of reproductive age with deep infiltrating endometriosis

In: Voprosy ginekologii, akušerstva i perinatologii · 2021 · vol. 20(6) , pp. 92–100 · doi:10.20953/1726-1678-2021-6-92-100 · W4285541090
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Deep infiltrating endometriosis is associated with diminished ovarian reserve, evidenced by fewer antral follicles, although no PIK3CA gene mutations were found in the tested tissues.

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This study evaluated ovarian reserve in 50 reproductive-age patients with deep infiltrating endometriosis using serum anti-Müllerian hormone (AMH), follicle-stimulating hormone, estradiol, and antral follicle count by transvaginal ultrasound, compared with 25 reproductive-age patients undergoing laparoscopic metroplasty of a post-cesarean uterine scar. AMH levels were lower on average in the endometriosis group but not significantly so (2.6 ± 2.2 vs 3.6 ± 3.5 ng/mL, p > 0.05), while antral follicle counts were significantly reduced in the endometriosis group overall (8.5 ± 4.5 vs 12.2 ± 4.1, p = 0.001), including both those with ovarian endometriomas and those without. Next-generation sequencing of ovarian endometrioma tissue (n = 18) and healthy ovarian tissue biopsies (n = 50 in the endometriosis group; n = 25 controls) found no activating PIK3CA mutations. This paper is centrally about endometriosis — deep infiltrating endometriosis and its association with diminished ovarian reserve, alongside assessment of PI3K/AKT/mTOR pathway mutations.

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Abstract

Objective. To study the effect of deep infiltrating endometriosis on the status of ovarian reserve in patients of reproductive age and to assess the spectrum of PIK3CA gene mutations among patients with infiltrating form of external genital endometriosis. Patients and methods. The study group included 50 patients of reproductive age with deep infiltrating endometriosis, of whom 18 had deep infiltrating endometriosis combined with ovarian endometriomas. The comparison group included 25 patients of reproductive age who underwent laparoscopic metroplasty of post-cesarean section uterine scar. In all patients, serum levels of anti-mullerian hormone (AMH), follicle-stimulating hormone, and estradiol were determined by enzyme immunoassay, and an antral follicle count in the ovaries was done via transvaginal ultrasound. The search for activating mutations in the PIK3CA gene was performed by next-generation DNA sequencing in the samples of ovarian endometriomas from patients with a combination of infiltrating endometriosis and endometrioid cysts (n = 18) and in biopsy samples of healthy ovarian tissue from all patients in the study (n = 50) and comparison groups (n = 25). Results. Evaluation of the ovarian reserve status in patients from two groups showed that levels of AMH were lower in patients with infiltrating form of external genital endometriosis than in the comparison group by 1.0 ng/mL on average (2.6 ± 2.2 ng/mL in the study group, 3.6 ± 3.5 ng/mL in the comparison group), but the difference was not statistically significant, p > 0.05. The number of antral follicles according to transvaginal ultrasound was significantly lower in the study group (8.5 ± 4.5) than in the comparison group (12.2 ± 4.1), p = 0.001. This difference was statistically significant both for patients with ovarian endometriomas (6.0 ± 4.2, p < 0.001) and for patients without ovarian endometrioid tumors (9.8 ± 4.2, p = 0.04). Our study did not detect PIK3CA gene mutations in any of the ovarian endometrioma tissue samples from patients with a combination of infiltrating endometriosis and endometrioid cysts, and in none of the healthy ovarian tissue biopsy samples from patients in the study and comparison groups. Conclusion. Thus, the presence of deep infiltrating endometriosis is associated with diminished ovarian reserve in patients of reproductive age, regardless of the presence of ovarian endometrioid tumors. Population studies are needed to detect PIK3CA gene mutations in endometriosis, as well as to investigate mutations in other genes encoding regulatory proteins of the PI3K/AKT/mTOR anti-apoptotic signaling pathway to reveal the mechanisms of ovarian reserve depletion in case of infiltrating forms of external genital endometriosis. Key words: infertility, deep infiltrating endometriosis, ovarian reserve, PI3K/AKT/mTOR signaling pathway, ovarian endometrioma
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Activating mutations of genes in the PI3K/AKT/mTOR signaling pathway and ovarian reserve status in patients of reproductive age with deep infiltrating endometriosis Ekaterina O. Okulova / Oksana A. Melkozerova / Artur A. Mikhelson / Galina B. Malgina / Tatyana B. Tretyakova / Tatiana A. Putilova / Objective. To study the effect of deep infiltrating endometriosis on the status of ovarian reserve in patients of reproductive age and to assess the spectrum of PIK3CA gene mutations among patients with infiltrating form of external genital endometriosis. Patients and methods. The study group included 50 patients of reproductive age with deep infiltrating endometriosis, of whom 18 had deep infiltrating endometriosis combined with ovarian endometriomas. The comparison group included 25 patients of reproductive age who underwent laparoscopic metroplasty of post-cesarean section uterine scar. In all patients, serum levels of anti-mullerian hormone (AMH), follicle-stimulating hormone, and estradiol were determined by enzyme immunoassay, and an antral follicle count in the ovaries was done via transvaginal ultrasound. The search for activating mutations in the PIK3CA gene was performed by next-generation DNA sequencing in the samples of ovarian endometriomas from patients with a combination of infiltrating endometriosis and endometrioid cysts (n = 18) and in biopsy samples of healthy ovarian tissue from all patients in the study (n = 50) and comparison groups (n = 25). Results. Evaluation of the ovarian reserve status in patients from two groups showed that levels of AMH were lower in patients with infiltrating form of external genital endometriosis than in the comparison group by 1.0 ng/mL on average (2.6 ± 2.2 ng/mL in the study group, 3.6 ± 3.5 ng/mL in the comparison group), but the difference was not statistically significant, p > 0.05. The number of antral follicles according to transvaginal ultrasound was significantly lower in the study group (8.5 ± 4.5) than in the comparison group (12.2 ± 4.1), p = 0.001. This difference was statistically significant both for patients with ovarian endometriomas (6.0 ± 4.2, p < 0.001) and for patients without ovarian endometrioid tumors (9.8 ± 4.2, p = 0.04). Our study did not detect PIK3CA gene mutations in any of the ovarian endometrioma tissue samples from patients with a combination of infiltrating endometriosis and endometrioid cysts, and in none of the healthy ovarian tissue biopsy samples from patients in the study and comparison groups. Conclusion. Thus, the presence of deep infiltrating endometriosis is associated with diminished ovarian reserve in patients of reproductive age, regardless of the presence of ovarian endometrioid tumors. Population studies are needed to detect PIK3CA gene mutations in endometriosis, as well as to investigate mutations in other genes encoding regulatory proteins of the PI3K/AKT/mTOR anti-apoptotic signaling pathway to reveal the mechanisms of ovarian reserve depletion in case of infiltrating forms of external genital endometriosis. Key words: infertility, deep infiltrating endometriosis, ovarian reserve, PI3K/AKT/mTOR signaling pathway, ovarian endometrioma For citation: Okulova O.E., Melkozerova O.A., Mikhelson A.A., Malgina G.B., Tretyakova T.B., Putilova T.A. Activating mutations of genes in the PI3K/AKT/mTOR signaling pathway and ovarian reserve status in patients of reproductive age with deep infiltrating endometriosis. Vopr. ginekol. akus. perinatol. (Gynecology, Obstetrics and Perinatology). 2021; 20(6): 92–100. (In Russian). DOI: 10.20953/1726-1678-2021-6-92-100

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