Mild experimental increase in testis and epididymis temperature in men: effects on sperm morphology according to spermatogenesis stages

Abstract

Background: A mild increase in testicular and epididymal temperatures in men, bulls and rams (pendulous scrotum) inhibits spermatogenesis and increases the percentage of sperm with an abnormal morphology. However, the stages of spermatogenesis that are most sensitive to a mild increase in testicular temperature in men are unknown. The aim of the present study was to explore the effects of a mild induced increase in testicular and epididymal temperature (i.e., testicular temperature maintained below the core body temperature) on sperm morphology in humans depending on the physiological time of spermatogenesis and epididymal transit.

Methods: Five healthy volunteers were enrolled in an experimental study in which testicular and epididymal temperatures were increased by maintaining the testes in a supra-scrotal position with a specially designed underwear worn 15±1 h a day for 120 consecutive days. Semen collection was scheduled on specific days depending on spermatogenic stages and epididymal transit.

Results: Sperm morphology and the multiple anomalies index (MAI) were analysed before, during and after heating. This mild induced increase in testicular and epididymal temperatures resulted in a significant rise in the percentage of morphologically abnormal spermatozoa on day 34 of heating, which remained elevated throughout the heating period and persisted until 45 days after cessation of heating. The MAI was significantly increased on day 20 throughout the heating period and persisted 45 days after cessation of heating. An increase in the percentage of anomalies in the sperm head, acrosome or tail occurred on days 34 and/or 45 of heating. Abnormal sperm morphology and MAI reverted to control values 73 days after cessation of heating.

Conclusions: A mild sustained increase in testicular and epididymal temperature in man leads morphological abnormalities in spermatozoa mainly due to an impairment of spermiogenesis and meiosis.

Keywords: Men; meiosis; sperm morphology; spermiogenesis; testis temperature.

Figure 1

Chronology of semen sampling. (A) Diagram to illustrate the timing of semen sampling during the three study periods before, during and after heating (phase I, phase II); (B) location and evolutionary stages of sperm during the spermatogenic process at heat induction (D0) and their expected appearance in ejaculates. E = epididymal sperm; T = spermatids; C2 = spermatocytes II; C1 = spermatocytes I; G = spermatogonia; SC = stem cells (adapted from: Mild induced testicular and epididymal hyperthermia alters sperm chromatin integrity in men, Fertility and Sterility 2012 with permission from Elsevier).

Figure 2

Percentages of spermatozoa with normal morphology, MAI sperm count (millions/mL) and semen volume (mL) before, during, and after (phase I and phase II) mild induced testicular and epididymal heating in men (n=5). (A) Percentages of spermatozoa with normal morphology, MAI; (B) sperm count (millions/mL) and semen volume (mL). Means ± SEM were represented compared to the control group (control; n=27). *, P<0.05. Grey zona: sperm morphology study not possible (see results). MAI, multiple anomalies index; SEM, standard error of the mean.

Figure 3

Description of increase in some specific sperm morphology anomalies during and after (phase I and phase II) mild induced testicular and epididymal heating in men: (A) head abnormalities; (B) acrosome-related abnormalities; (C) tail abnormalities. Data concerning fold increase in sperm anomalies during and after heating were compared to baseline mean values at −40, −15 and 0 day before heating. Grey zona: analyses between day 73 and day 154 were not possible (see results).

Figure 4

Diagram to illustrate the number of volunteers with a higher percentage of abnormalities during and after mild induced testicular and epididymal heating than at baseline before heating (see results) and which correspond to the spermatogenesis stage and epididymal transit heating chronology. Each cell represents one volunteer. For one anomaly, a blue cell means that a volunteer has an abnormal percentage. A white cell means that a volunteer has a normal percentage. A green cell means that the stages of spermatogenesis or epididymis were not heated. A red cell means that the stages of spermatogenesis or epididymis were heated.

Figure S1

Presentation of the effects of a mild testicular temperature increase on sperm morphology in men, bulls and rams according to the duration of epididymis transit and stages of spermatogenesis (8,13,14,16-21,26-28,43-45,53). Animal studies used scrotal insulation. Red squares represent heating periods. Orange squares represent a significant effect on sperm morphology. White squares represent an absence of significant effect. In: during heating; AF: after heating; STP: duration of spermatogenesis; ST: scrotal temperature. *, ST: no scrotal or testicular temperature measurement.