Analysis of hormonal status and the course of endometriosis in patients with type 1 diabetes mellitus

In: Journal of obstetrics and women's diseases · 2025 · vol. 73(6) , pp. 101–115 · doi:10.17816/jowd636594 · W4406924940
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This study found that women with type 1 diabetes and endometriosis had lower anti-Müllerian hormone and vitamin D levels, and progesterone levels comparable to endometriosis patients but lower than controls.

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This prospective clinical study evaluated hormonal status, vitamin D levels (25-hydroxycalciferol), and aspects of the clinical course of endometriosis in 339 women, including groups with type 1 diabetes mellitus (T1D) alone, T1D combined with laparoscopically verified endometriosis, endometriosis alone, and healthy controls. Across three consecutive menstrual cycles, serum anti-Müllerian hormone, gonadotropins, prolactin, and estradiol/progesterone were measured, and T1D participants had glycated hemoglobin assessed; endometriosis severity was stratified by prevalence grades. Compared with other groups, the T1D plus endometriosis group had the lowest vitamin D, while anti-Müllerian hormone was reduced in the endometriosis group relative to other groups; progesterone was lower than controls in all groups, and glycated hemoglobin was higher in T1D participants. Grades III–IV were more common without T1D, and deep infiltrating endometriosis and reoperations were more frequent in the endometriosis-only group, with the paper noting that an asymptomatic preclinical period in T1D could contribute to delayed diagnosis and treatment. This paper is centrally about endometriosis — it analyzes how type 1 diabetes mellitus modifies hormonal status, vitamin D, and the clinical course of endometriosis, including severity features verified by laparoscopy and histology.

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Abstract

Background: Type 1 diabetes mellitus and endometriosis significantly reduce the quality of patient’s life and hinder the implementation of reproductive plans. Studying the features of the clinical course of endometriosis in patients with type 1 diabetes mellitus will help in the development of new effective and safe therapeutic strategies and diagnostic methods. Aim: The aim of this study was to analyze the clinical course of the diseases, hormonal status and blood vitamin D (25-hydroxycalciferol) levels in patients with type 1 diabetes mellitus combined with endometriosis. Materials and methods: This clinical prospective study included 339 women, of whom 79 patients were with type 1 diabetes mellitus combined with endometriosis (mean age 31.7 ± 5.0 years), 51 patients were with endometriosis (mean age 31.4 ± 3.7 years), and 209 patients were with type 1 diabetes mellitus (mean age 30.2 ± 4.9 years). The control group consisted of 31 healthy women of reproductive age. The immunochemiluminescent method was used to determine the blood serum levels of anti-Müllerian hormone, follicle-stimulating hormone, luteinizing hormone, prolactin, and estradiol (days 2–5 of the menstrual cycle), progesterone (days 20–23 of the menstrual cycle) during three consecutive menstrual cycles, and the blood serum level of glycated hemoglobin was also studied in patients with type 1 diabetes mellitus. The diagnosis of endometriosis in all patients was confirmed based on laparoscopic surgery with verification by histological examination. Results: When assessing the levels of gonadotropins, prolactin, and anti-Müllerian hormone in patients with endometriosis, a decrease in blood anti-Müllerian hormone level was noted in comparison with the other study groups. The levels of gonadotropins and prolactin in patients in all of the study groups were comparable. In all of the study groups, the progesterone level on days 20–23 of the cycle was lower than in the control group. The concentration of vitamin D (25-hydroxycalciferol) in the patients’ peripheral blood in all of the study groups was lower compared to the control group, with the minimum value of 16.3 ± 4.1 ng/ml found in the group of patients with type 1 diabetes mellitus combined with endometriosis. In patients with type 1 diabetes mellitus and in those with the disease combined with endometriosis, no differences were found between the age of onset of type 1 diabetes mellitus and its duration, the total daily insulin dose, and the insulin dose per kilogram of the patient’s weight. The glycated hemoglobin level was higher in the group of patients with type 1 diabetes mellitus. When distributing patients by the grades of endometriosis prevalence, it was found that grades III and IV were more common in patients without type 1 diabetes mellitus. The incidence of deep infiltrating endometriosis was higher in the group of patients with endometriosis only, as was the number of reoperations. Conclusions: The asymptomatic preclinical period of endometriosis in patients with type 1 diabetes mellitus may lead to untimely and erroneous diagnosis and delayed treatment of the disease. In patients with type 1 diabetes mellitus onset in puberty and suffering from endometriosis, the risk of vascular complications increases and the ovarian reserve decreases, which requires the implementation of reproductive goals as early as possible. When choosing therapy for endometriosis in patients with type 1 diabetes mellitus, the presence of vascular complications should be taken into account.
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Abstract

Background: Type 1 diabetes mellitus and endometriosis significantly reduce the quality of patient’s life and hinder the implementation of reproductive plans. Studying the features of the clinical course of endometriosis in patients with type 1 diabetes mellitus will help in the development of new effective and safe therapeutic strategies and diagnostic methods. Aim: The aim of this study was to analyze the clinical course of the diseases, hormonal status and blood vitamin D (25-hydroxycalciferol) levels in patients with type 1 diabetes mellitus combined with endometriosis.

Materials and methods

This clinical prospective study included 339 women, of whom 79 patients were with type 1 diabetes mellitus combined with endometriosis (mean age 31.7 ± 5.0 years), 51 patients were with endometriosis (mean age 31.4 ± 3.7 years), and 209 patients were with type 1 diabetes mellitus (mean age 30.2 ± 4.9 years). The control group consisted of 31 healthy women of reproductive age. The immunochemiluminescent method was used to determine the blood serum levels of anti-Müllerian hormone, follicle-stimulating hormone, luteinizing hormone, prolactin, and estradiol (days 2–5 of the menstrual cycle), progesterone (days 20–23 of the menstrual cycle) during three consecutive menstrual cycles, and the blood serum level of glycated hemoglobin was also studied in patients with type 1 diabetes mellitus. The diagnosis of endometriosis in all patients was confirmed based on laparoscopic surgery with verification by histological examination.

Results

When assessing the levels of gonadotropins, prolactin, and anti-Müllerian hormone in patients with endometriosis, a decrease in blood anti-Müllerian hormone level was noted in comparison with the other study groups. The levels of gonadotropins and prolactin in patients in all of the study groups were comparable. In all of the study groups, the progesterone level on days 20–23 of the cycle was lower than in the control group. The concentration of vitamin D (25-hydroxycalciferol) in the patients’ peripheral blood in all of the study groups was lower compared to the control group, with the minimum value of 16.3 ± 4.1 ng/ml found in the group of patients with type 1 diabetes mellitus combined with endometriosis. In patients with type 1 diabetes mellitus and in those with the disease combined with endometriosis, no differences were found between the age of onset of type 1 diabetes mellitus and its duration, the total daily insulin dose, and the insulin dose per kilogram of the patient’s weight. The glycated hemoglobin level was higher in the group of patients with type 1 diabetes mellitus. When distributing patients by the grades of endometriosis prevalence, it was found that grades III and IV were more common in patients without type 1 diabetes mellitus. The incidence of deep infiltrating endometriosis was higher in the group of patients with endometriosis only, as was the number of reoperations.

Conclusions

The asymptomatic preclinical period of endometriosis in patients with type 1 diabetes mellitus may lead to untimely and erroneous diagnosis and delayed treatment of the disease. In patients with type 1 diabetes mellitus onset in puberty and suffering from endometriosis, the risk of vascular complications increases and the ovarian reserve decreases, which requires the implementation of reproductive goals as early as possible. When choosing therapy for endometriosis in patients with type 1 diabetes mellitus, the presence of vascular complications should be taken into account. Full Text About the authors Elena V. Misharina The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O.Ott Author for correspondence. Email: [email protected] ORCID iD: 0000-0002-0276-7112 SPIN-code: 7350-5674 MD, Cand. Sci. (Medicine) Russian Federation, Saint PetersburgAlena V. Tiselko The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O.Ott Email: [email protected] ORCID iD: 0000-0002-2512-833X SPIN-code: 5644-9891 MD, Dr. Sci. (Medicine) Russian Federation, Saint PetersburgMaria I. Yarmolinskaya The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O.Ott Email: [email protected] ORCID iD: 0000-0002-6551-4147 SPIN-code: 3686-3605 MD, Dr. Sci. (Medicine), Professor, Professor of the Russian Academy of Sciences Russian Federation, Saint PetersburgReferences - Magliano DJ, Boyko EJ; IDF Diabetes Atlas 10th edition scientific committee. IDF diabetes atlas. 10th edition. Brussels: International Diabetes Federation; 2021. [cited 2024 Nov 28] Available from: https://www.ncbi.nlm.nih.gov/books/NBK581934/ - DiMeglio LA, Evans-Molina C, Oram RA. Type 1 diabetes. Lancet. 2018;391(10138):2449–2462. doi: 10.1016/S0140-6736(18)31320-5 - Norris JM, Johnson RK, Stene LC. Type 1 diabetes-early life origins and changing epidemiology. Lancet Diabetes Endocrinol. 2020;8(3):226–238. doi: 10.1016/S2213-8587(19)30412-7 - Rogers MAM, Kim C, Banerjee T, et al. Fluctuations in the incidence of type 1 diabetes in the United States from 2001 to 2015: a longitudinal study. BMC Med. 2017;15(1):199. doi: 10.1186/s12916-017-0958-6 - Harding JL, Wander PL, Zhang X, et al. The incidence of adult-onset type 1 diabetes: a systematic review from 32 countries and regions. Diabetes Care. 2022;45(4):994–1006. doi: 10.2337/dc21-1752 - Dedov II, Shestakova MV, Vikulova OK, et al. Epidemiological characteristics of diabetes mellitus in the Russian Federation: clinical and statistical analysis according to the Federal diabetes register data of 01.01.2021. Diabetes mellitus. 2021;24(3):204–221. EDN: MEZKMG doi: 10.14341/DM12759 - Whitworth KW, Baird DD, Stene LC, et al. Fecundability among women with type 1 and type 2 diabetes in the Norwegian mother and child cohort study. Diabetologia. 2011;54:516–522. doi: 10.1007/s00125-010-2003-6 - Yarmolinskaya MI, Ailamazyan EK. Genital endometriosis. Various aspects of the problem. Saint Petersburg: Eco-Vector; 2017. 615 p. EDN: XYSZVJ (In Russ.) - Taylor HS, Kotlyar AM, Flores VA. Endometriosis is a chronic systemic disease: clinical challenges and novel innovations. Lancet. 2021;397(10276):839–852. doi: 10.1016/S0140-6736(21)00389-5 - Vaduva P, Laouali N, Fagherazzi G, et al. Association between endometriosis and risk of type 2 diabetes: results from the prospective E3N cohort. Maturitas. 2023;177:107805. doi: 10.1016/j.maturitas.2023.107805 - Farland LV, Degnan WJ, Harris HR, et al. A prospective study of endometriosis and risk of type 2 diabetes. Diabetologia. 2021;64(3):552–560. doi: 10.1007/s00125-020-05347-6 - Pérez-López FR, Martínez-Domínguez SJ, Viñas A, et al. Endometriosis and gestational diabetes mellitus risk: a systematic review and meta-analysis. Gynecol Endocrinol. 2018;34(5):363–369. doi: 10.1080/09513590.2017.1397115 - Salmeri N, Li Piani L, Cavoretto PI, et al. Endometriosis increases the risk of gestational diabetes: a meta-analysis stratified by mode of conception, disease localization and severity. Sci Rep. 2023;13(1):8099. doi: 10.1038/s41598-023-35236-y - Andreeva NY, Yarmolinskaya MI, Misharina EV, et al. The potential of survivin as a non-invasive diagnostic marker for endometriosis in patients with type 1 diabetes mellitus. Journal of Obstetrics and Women’s Diseases. 2023;72(6):5–15. EDN: XLJYVP doi: 10.17816/JOWD567975 - Xin Q, Li HJ, Chen HK, et al. Causal effects of glycemic traits and endometriosis: a bidirectional and multivariate mendelian randomization study. Diabetol Metab Syndr. 2024;16(1):77. doi: 10.1186/s13098-024-01311-1 - Simmen RCM, Brown DM, Quick CM, et al. Co-morbidity of type 1 diabetes and endometriosis: bringing a new paradigm into focus. J Endocrinol. 2019;243(3):R47–R57. doi: 10.1530/joe-19-0248 - Osum KC, Burrack AL, Martinov T, et al. Interferon-gamma drives programmed death-ligand 1 expression on islet β cells to limit T cell function during autoimmune diabetes. Sci Rep. 2018;8(1):8295. doi: 10.1038/s41598-018-26471-9 - Gueuvoghlanian-Silva BY, Bellelis P, Barbeiro DF, et al. Treg and NK cells related cytokines are associated with deep rectosigmoid endometriosis and clinical symptoms related to the disease. J Reprod Immunol. 2018;126:32–38. doi: 10.1016/j.jri.2018.02.003 - Kocbek V, Grandi G, Blank F, et al. TNFα-induced IKKβ complex activation influences epithelial, but not stromal cell survival in endometriosis. Mol Hum Reprod. 2016;22(11):768–777. doi: 10.1093/molehr/gaw054 - Khan KN, Kitajima M, Inoue T, et al. Additive effects of inflammation and stress reaction on toll-like receptor 4-mediated growth of endometriotic stromal cells. Hum Reprod. 2013;28(10):2794–2803. doi: 10.1093/humrep/det280 - Alhallak I, Quick CM, Graham GL, et al. A pilot study on the co-existence of diabetes and endometriosis in reproductive-age women: potential for endometriosis progression. Reprod Sci. 2023;30(8):2429–2438. doi: 10.1007/s43032-023-01190-3 - Martel J, Chang SH, Ko YF, et al. Gut barrier disruption and chronic disease. Trends Endocrinol Metab. 2022;33(4):247–265. doi: 10.1016/j.tem.2022.01.002 - Patterson E, Ryan PM, Cryan JF, et al. Gut microbiota, obesity and diabetes. Postgrad Med J. 2016;92(1087):286–300. doi: 10.1136/postgradmedj-2015-133285 - Patent RUS № 2693050/ 11.09.2018. Jarmolinskaja MI, Molotkov AS, Thazaplezheva SSh. Sposob lechenija naruzhnogo genital’nogo jendometrioza. (In Russ.) EDN: UEBVQN [cited 2024 Nov 28] Available from: https://patents.s3.yandex.net/RU2693050C1_20190701.pdf. - Zaimi M, Michalopoulou O, Stefanaki K, et al. Gonadal dysfunction in women with diabetes mellitus. Endocrine. 2024;85(2):461–472. doi: 10.1007/s12020-024-03729-z - Deltsidou A, Lemonidou C, Zarikas V, et al. Oligomenorrhoea in adolescents with type 1 diabetes mellitus: relationship to glycemic control. Eur J Obstet Gynecol Reprod Biol. 2010;153:62–66. doi: 10.1016/j.ejogrb.2010.07.027 - Nishikawa-Nakamura N, Kawamura T, Nakamichi T, et al. Age at menarche in Japanese patients with type 1 diabetes mellitus: a look at changes since 1960s. Endocr J. 2022;69(6):627–633. doi: 10.1507/endocrj.EJ21-0533 - Harjutsalo V, Maric-Bilkan C, Forsblom C, et al; FinnDiane Study Group. Age at menarche and the risk of diabetic microvascular complications in patients with type 1 diabetes. Diabetologia. 2016;59(3):472–480. doi: 10.1007/s00125-015-3816-0 - Tolpygina MG, Tarasova MA, Borovik NV, et al. Effect of diabetes compensation on ovarian function recovery in women of reproductive age with type 1 diabetes mellitus. Journal of Obstetrics and Women’s Diseases. 2018;67(5):42–49. EDN: YPHWXJ doi: 10.17816/JOWD67542-49 - Meshkova IP, Grigorjan OR, Zilov AV, et al. The role of autoantibodies to ovarian and adrenal tissue in the pathogenesis of menstrual cycle disorders in girls with type I diabetes mellitus. Russian Journal of Human Reproduction. 2000;(5):11–15. (In Russ.) EDN: PXVTXN - Poteen VV, Borovik NV, Tiselko AV. Diabetes mellitus and female reproductive system. Journal of Obstetrics and Women’s Diseases. 2006;55(1):85–89. EDN: HZNTJV - Shebl O, Ebner T, Sommergruber M, et al. Anti-muellerian hormone serum levels in women with endometriosis: a case–control study. Gynecol Endocrinol. 2009;25(11):713–716. doi: 10.3109/09513590903159615 - Molotkov AS, Yarmolinskaya MI. A role of anti-Mullerian hormone in external genital endometriosis. Obstetrics, Gynecology and Reproduction. 2021;15(2):182–188. EDN: TPJXBJ doi: 10.17749/2313-7347/ob.gyn.rep.2021.164 - Kim YJ, Cha SW, Kim HO. Serum anti-Müllerian hormone levels decrease after endometriosis surgery. J Obstet Gynaecol. 2017;37(3):342–346. doi: 10.1080/01443615.2016.1239071 - Coccia ME, Rizzello F, Capezzuoli T., et al. Bilateral endometrioma excision: surgery-related damage to ovarian reserve. Reprod Sci. 2019;26(4):543–550. doi: 10.1177/1933719118777640 - Zhang C, Li X, Dai Y, et al. Risk factors associated with changes in serum anti-Müllerian hormone levels before and after laparoscopic cystectomy for endometrioma. Front Endocrinol. 2024;15:1359649. doi: 10.3389/fendo.2024.1359649. - Daniilidis A, Grigoriadis G, Kalaitzopoulos DR, et al. Surgical management of ovarian endometrioma: impact on ovarian reserve parameters and reproductive outcomes. J Clin Med. 2023;12(16):5324. doi: 10.3390/jcm12165324. - Kacem-Berjeb K, Braham M, Massoud CB, et al. Does endometriosis impact the composition of follicular fluid in IL6 and AMH? A case-control study. J Clin Med. 2023;12(5):1829. doi: 10.3390/jcm12051829 - Yang W, Lin C, Zhang M, et al. Assessment of ovarian reserve in patients with type 1 diabetes: a systematic review and meta-analysis. Endocrine. 2022;77(2):205–212. doi: 10.1007/s12020-022-03091-y - Kadiroğullar P, Demir E, Bahat PY, et al. Evaluation of relationship between HbA1c levels and ovarian reserve in patients with type 1 diabetes mellitus. Gynecol Endocrinol. 2020;36(5):426–430. doi: 10.1080/09513590.2019.1708893 - Kim C, Dunn RL, Braffett B; EDIC Research Group. Ovarian reserve in women with Type 1 diabetes in the diabetes control and complications trial/epidemiology of diabetes interventions and complications study. Diabet Med. 2016;33(5):691–692. doi: 10.1111/dme.13072 - Denisova AS, Yarmolinskaya MI. The role of vitamin D in the pathogenesis of genital endometriosis. Journal of Obstetrics and Women’s Diseases. 2017;66(6):81–88. EDN: YKWEDH doi: 10.17816/JOWD66681-88 (In Russ.) - Ciavattini A, Serri M, Delli Carpini G, et al. Ovarian endometriosis and vitamin D serum levels. Gynecol Endocrinol. 2017;33(2):164–167. doi: 10.1080/09513590.2016.1239254 - Federico G, Genoni A, Puggioni A, et al. Vitamin D status, enterovirus infection, and type 1 diabetes in Italian children/adolescents. Pediatr Diabetes. 2018;19(5):923–929. doi: 10.1111/pedi.12673 - Felício KM, de Souza ACCB, Neto JFA, et al. Glycemic variability and insulin needs in patients with type 1 diabetes mellitus supplemented with vitamin D: a pilot study using continuous glucose monitoring system. Curr Diabet Rev. 2018;14(4):395–403. doi: 10.2174/1573399813666170616075013 - Sørensen IM, Joner G, Jenum PA, t al. Maternal serum levels of 25-hydroxy-vitamin D during pregnancy and risk of type 1 diabetes in the offspring. Diabetes. 2012;61(1):175–178. doi: 10.2337/db11-0875 - Zhang J, Upala S, Sanguankeo A. Relationship between vitavin D deficiency and diabetic retinopathy: a meta-analysis. Can J Ophthalmol. 2016;52:S39–S44. doi: 10.1016/jcjo.2016.10.004 - Mormile R, Vittori G. Type 1 diabetes in women with endometriosis: what is the risk of occurence? Pediatr Edocr Met. 2013;24(9–10):1007–1008. doi: 10.1525/ipem-2013-0134 - Yarmolinskaya MI, Abashova EI, Misharina EV, et al. Drug therapy of genital endometriosis: realities and prospects: a guide for doctors / edited by M.I. Yarmolinskaya. Moscow: GEOTAR-Media; 2021. (In Russ.) EDN: VWPPLC doi: 10.33029/9704-6034-4-МЕТ-2021-1-384 - Hernández A, Sanz A, Spagnolo E, et al. Impact of ovarian endometrioma and surgery on reproductive outcomes: a single-center Spanish cohort study. Biomedicines. 2023;11(3):844. doi: 10.3390/biomedicines11030844 - Larsen MD, Jensen DM, Fedder J, et al. Live-born children after assisted reproduction in women with type 1 diabetes and type 2 diabetes: a nationwide cohort study. Diabetologia. 2020;63(9):1736–1744. doi: 10.1007/s00125-020-05193-6 - Misharina EV, Tiselko AV, Yarmolinskaya MI, et al. In vitro fertilization as a method of infertility treatment in women with type 1 diabetes mellitus. Diabetes mellitus. 2018;21(5):425–430. EDN: YPVIOT doi: 10.14341/DM9573 (In Russ.) - Misharina EV, Yarmolinskaya MI, Borovik NV. Algorithms of preparation for art programs in patients with type 1 diabetes mellitus. Obstetrics and Gynegology. 2022;(S9):50–56. (In Russ.)

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