Independent and combined effects of diethylhexyl phthalate and polychlorinated biphenyl 153 on sperm quality in the human and dog

Abstract

A temporal decline in human and dog sperm quality is thought to reflect a common environmental aetiology. This may reflect direct effects of seminal chemicals on sperm function and quality. Here we report the effects of diethylhexyl phthalate (DEHP) and polychlorinated biphenyl 153 (PCB153) on DNA fragmentation and motility in human and dog sperm. Human and dog semen was collected from registered donors (n = 9) and from stud dogs (n = 11) and incubated with PCB153 and DEHP, independently and combined, at 0x, 2x, 10x and 100x dog testis concentrations. A total of 16 treatments reflected a 4 × 4 factorial experimental design. Although exposure to DEHP and/or PCB153 alone increased DNA fragmentation and decreased motility, the scale of dose-related effects varied with the presence and relative concentrations of each chemical (DEHP.PCB interaction for: DNA fragmentation; human p < 0.001, dog p < 0.001; Motility; human p < 0.001, dog p < 0.05). In both human and dog sperm, progressive motility negatively correlated with DNA fragmentation regardless of chemical presence (Human: P < 0.0001, r = -0.36; dog P < 0.0001, r = -0.29). We conclude that DEHP and PCB153, at known tissue concentrations, induce similar effects on human and dog sperm supporting the contention of the dog as a sentinel species for human exposure.

Figure 1

Effect of DEHP and PCB153 on dog and human sperm motility. Chemicals tested individually [ai,bi: PCB only; aii,bii: grey bars: DEHP only] and in combination [aii,bii]. Graphs display fixed concentrations of DEHP with increasing concentrations of PCB153 in dog [ai,aii: p <  0.01] and human [bi,bii: p <  0.001] sperm. Grade a motility: >25 μm/s Error bar = 1 Standard Error of Difference. MTC = Mean testis concentration.

Figure 2

Effect of DEHP and PCB153 on dog and human sperm DNA fragmentation. Chemicals tested individually [ai,bi: PCB only; aii,bii: grey bars: DEHP only] and in combination [aii,bii]. Graphs display fixed concentrations of DEHP with increasing concentrations of PCB153 in dog [ai,aii: p ≤ 0.001] and human [bi,bii: p ≤ 0.001] sperm. Error bar = 1 Standard Error of difference between means. MTC = Mean testis concentration.

Figure 3

Correlation between progressive motility and DNA fragmentation in both dog and human sperm. Values from 32 sperm assessments (16 treatments, two time points). Each point represents a different sperm culture equating to a total n = 352 [dog] and n = 288 [human]. Colours denote culture media constituents to demonstrate spread: Control (black), DEHP (red), PCB153 (blue) and mixture (green). Dog (i, n = 352): Control; p < 0.05, r = −0.527, n = 22; DEHP; p < 0.05, r = −0.2862, n = 66; PCB153; p < 0.01, r = −0.3276, n = 66; Mixture; p < 0.0001, r = −0.2826, n = 198; vs Human (ii, n = 288): Control; p > 0.05, r = −0.4374, n = 18; DEHP; p < 0.05, r = −0.3118, n = 54; PCB153; p < 0.05, r = −0.2994, n = 54; Mixture; p < 0.0001, r = −0.4037, n = 162]. Confidence bands (95%) plotted for visual purposes only. Progressive motility based on WHO pre-2010 where sperm swimming grades a and b are combined: ≥5 µm/s.