Investigating discordance between embryologists and histopathologists: analysis of multiple factors in mTESE sperm retrieval outcomes

Investigando la discordancia entre embriólogos e histopatólogos: análisis de múltiples factores en los resultados de recuperación de esperma mediante mTESE

The objective of the study is to primarily highlight the consistency between the embryologist and the histopathologist in microdissection testicular sperm extraction and to explore the factors affecting sperm retrieval. The research included 91 patients, aged 20 to 47, who visited our Reproductive Technology center from July 2020 to June 2023. Patient data were collected retrospectively, including demographics, physical exams, lab tests, radiological assessments, genetic analyses, medical histories and histopathological results. Using the Johnsen scoring system for evaluation, the histopathologist identified mature spermatozoa in the specimen in some patients (Johnsen score 8–10); however, the embryologist only declared successful sperm retrieval in 66.6% of them. Overall sperm retrieval rates were lower than expected at 40%. Significant factors influencing sperm retrieval rates included Follicle Stimulating Hormone (p = 0.001), Luteinizing Hormone (p = 0.007), testicular volume (p < 0.001), histopathology (p < 0.001), and alcohol consumption (p = 0.007). A logistic regression model was used to identify the independent predictors of successful sperm retrieval. FSH (p = 0.038), testicular volume (p < 0.001), histopathology (p < 0.001), and alcohol consumption (p = 0.013) emerged as significant predictive factors for the outcome of sperm retrieval. As a result, in addition to patient-related factors, the consistency between the pathologist and embryologist also affects sperm retrieval rates.

Resumen

El objetivo del estudio es destacar principalmente la consistencia entre el embriólogo y el histopatólogo en la extracción de espermatozoides testiculares por microdisección y explorar los factores que afectan la recuperación de espermatozoides. La investigación incluyó a 91 pacientes, de 20 a 47 años, que visitaron nuestro centro de Tecnología Reproductiva desde julio de 2020 hasta junio de 2023. Se recopilaron datos retrospectivamente, incluyendo datos demográficos, exámenes físicos, pruebas de laboratorio, evaluaciones radiológicas, análisis genéticos, historias médicas y resultados histopatológicos. Utilizando el sistema de puntuación de Johnsen para la evaluación, el histopatólogo identificó espermatozoides maduros en la muestra en algunos pacientes (puntuación de Johnsen 8–10); sin embargo, el embriólogo solo declaró recuperación exitosa de espermatozoides en el 66.6% de ellos. En general, las tasas de recuperación de espermatozoides fueron más bajas de lo esperado, con un 40%. Los factores significativos que afectaron las tasas de recuperación de espermatozoides incluyeron Hormona Folículo Estimulante (p = 0.001), Hormona Luteinizante (p = 0.007), volumen testicular (p < 0.001), histopatología (p < 0.001) y consumo de alcohol (p = 0.007). Se utilizó un modelo de regresión logística para identificar los predictores independientes de la recuperación exitosa de espermatozoides. FSH (p = 0.038), volumen testicular (p < 0.001), histopatología (p < 0.001) y consumo de alcohol (p = 0.013) surgieron como factores predictivos significativos para el resultado de la recuperación de espermatozoides. Por lo tanto, además de los factores relacionados con el paciente, la consistencia entre el patólogo y el embriólogo también afecta las tasas de recuperación de espermatozoides.

Azoospermia; mTESE; Histopathology; Embriyology; Sperm retrieval

Palabras Clave

Azoospermia; mTESE; Histopatología; Embriología; Recuperación espermática

[1] Takeshima T, Karibe J, Saito T, Kuroda S, Komeya M, Uemura H, et al. Clinical management of nonobstructive azoospermia: an update. International Journal of Urology. 2024; 31: 17–24.

[2] Practice Committee of the American Society for Reproductive Medicine in collaboration with the Society for Male Reproduction and Urology. The management of obstructive azoospermia: a committee opinion. Fertility and Sterility. 2019; 111: 873–880.

[3] Corona G, Minhas S, Giwercman A, Bettocchi C, Dinkelman-Smit M, Dohle G, et al. Sperm recovery and ICSI outcomes in men with non-obstructive azoospermia: a systematic review and meta-analysis. Human Reproduction Update. 2019; 25: 733–757.

[4] Rogers M, Major N, Edwards K, Simpson K. An examination of predictive markers for successful sperm extraction procedures: a linear model and systematic review. Asian Journal of Andrology. 2023; 25: 38–42.

[5] Puia D, Miron A, Radavoi D, Jinga V, Pricop C. Follicle-stimulating hormone and Inhibin B as predictors of successful sperm retrieval in men undergoing testicular sperm extraction: a review of 44 cases and meta-analysis. African Journal of Reproductive Health. 2023; 27: 51–59.

[6] Aboukhshaba A, Punjani N, Doukakis S, Schlegel PN. Anti-Müllerian hormone level as a predictor of sperm retrieval with microdissection testicular sperm extraction in nonobstructive azoospermia. Andrologia. 2021; 53: e14220.

[7] Scott RT, Hong KH, Werner MD, Forman EJ, Ruiz A, Cheng MC, et al. Embryology training for Reproductive Endocrine fellows in the clinical human embryology laboratory. Journal of Assisted Reproduction and Genetics. 2014; 31: 385–391.

[8] Paraskevi L, Antigoni S, Kleanthi G. Stress and anxiety levels in couples who undergo fertility treatment: a review of systematic reviews. Materia Socio-Medica. 2021; 33: 60–64.

[9] Herndon CC, Godart ES, Turek PJ. Testosterone levels among non-obstructive azoospermic patients 2 years after failed bilateral microdissection testicular sperm extraction: a nested case-cohort study. Journal of Assisted Reproduction and Genetics. 2022; 39: 1297–1303.

[10] Schlegel PN. Testicular sperm extraction: microdissection improves sperm yield with minimal tissue excision. Human Reproduction. 1999; 14: 131–135.

[11] Johnsen SG. Testicular biopsy score count—a method for registration of spermatogenesis in human testes: normal values and results in 335 hypogonadal males. Hormones. 1970; 1: 2–25.

[12] Achermann APP, Pereira TA, Esteves SC. Microdissection testicular sperm extraction (micro-TESE) in men with infertility due to nonobstructive azoospermia: summary of current literature. International Urology and Nephrology. 2021; 53: 2193–2210.

[13] Abushamma F, Alazab RS, Allouh MZ, Abu Shamleh R, Abu Alwafa R, Ghalayini I. Testicular histopathology and follicular stimulating hormone to predict fertility in nonobstructive azoospermia. To be published in Urologia. 2024. [Preprint].

[14] Cissen M, Meijerink AM, D’Hauwers KW, Meissner A, van der Weide N, Mochtar MH, et al. Prediction model for obtaining spermatozoa with testicular sperm extraction in men with non-obstructive azoospermia. Human Reproduction. 2016; 31: 1934–1941.

[15] Taitson PF, Mourthé A Filho, Radaelli MRM. Testicular sperm extraction in men with sertoli cell-only testicular histology—1680 cases. JBRA Assisted Reproduction. 2019; 23: 246–249.

[16] Yücel C, Budak S, Keskin MZ, Kisa E, Kozacioglu Z. Predictive factors of successful salvage microdissection testicular sperm extraction (mTESE) after failed mTESE in patients with non-obstructive azoospermia: long-term experience at a single institute. Archivio Italiano di Urologia, Andrologia. 2018; 90: 136–140.

[17] Cito G, Coccia ME, Dabizzi S, Morselli S, Della Camera PA, Cocci A, et al. Relevance of testicular histopathology on prediction of sperm retrieval rates in case of non-obstructive and obstructive azoospermia. Urologia. 2018; 85: 60–67.

[18] Banerjee K, Singla B, Agria K. Correlation of serum FSH and rate of testicular sperm retrieval in non-obstructive azoospermia. Indian Journal of Endocrinology and Metabolism. 2023; 27: 167–169.

[19] Deng CY, Liu DF, Zhao LM, Lin HC, Mao JM, Zhang Z, et al. Development of a predictive model for increasing sperm retrieval success by microdissection testicular sperm extraction in patients with nonobstructive azoospermia. Asian Journal of Andrology. 2023; 25: 598–603.

[20] Xu T, Peng L, Lin X, Li J, Xu W. Predictors for successful sperm retrieval of salvage microdissection testicular sperm extraction (TESE) following failed TESE in nonobstructive azoospermia patients. Andrologia. 2017; 49: e12642.

[21] Li H, Chen LP, Yang J, Li MC, Chen RB, Lan RZ, et al. Predictive value of FSH, testicular volume, and histopathological findings for the sperm retrieval rate of microdissection TESE in nonobstructive azoospermia: a meta-analysis. Asian Journal of Andrology. 2018; 20: 30–36.

[22] Kizilkan Y, Toksoz S, Turunc T, Ozkardes H. Parameters predicting sperm retrieval rates during microscopic testicular sperm extraction in nonobstructive azoospermia. Andrologia. 2019; 51: e13441.

[23] Tian RH, Chen HX, Zhao LY, Yang C, Li P, Wan Z, et al. Efficacy and safety study of microsurgical varicocelectomy in the treatment of non-obstructive azoospermia with varicocele. Chinese Medical Journal. 2018; 98: 3737–3740. (In Chinese)

[24] Çayan S, Orhan İ, Altay B, Aşcı R, Akbay E, Ayas B, et al. Fertility outcomes and predictors for successful sperm retrieval and pregnancy in 327 azoospermic men with a history of cryptorchidism who underwent microdissection testicular sperm extraction. Andrology. 2021; 9: 253–259.

[25] Arasteh H, Gilani MAS, Ramezani-Binabaj M, Babaei M. Microdissection testicular sperm extraction outcomes in azoospermic patients with bilateral orchidopexy. Andrology. 2024; 12: 157–163.

[26] Kang C, Punjani N, Kashanian JA, Schlegel PN. Age, sperm retrieval, and testicular histology in Klinefelter syndrome. The Journal of Urology. 2024; 211: 163–169.

[27] Özkan B, Coşkuner ER, Güdelci T. Predictive factors and intracytoplasmic sperm injection results for sperm retrieval by microdissection testicular sperm extraction (micro-TESE) in patients with Klinefelter syndrome. Urology. 2022; 161: 59–64.

[28] Colaco S, Modi D. Azoospermia factor c microdeletions and outcomes of assisted reproductive technology: a systematic review and meta-analysis. Fertility and Sterility. 2024; 121: 63–71.

[29] Abur U, Gunes S, Ascı R, Altundag E, Akar OS, Ayas B, et al. Chromosomal and Y-chromosome microdeletion analysis in 1,300 infertile males and the fertility outcome of patients with AZFc microdeletions. Andrologia. 2019; 51: e13402.

[30] Sengupta P, Nwagha U, Dutta S, Krajewska-Kulak E, Izuka E. Evidence for decreasing sperm count in African population from 1965 to 2015. African Health Sciences. 2017; 17: 418–427.